MA04CH20-Richards
ARI
ANNUAL
REVIEWS
3 November 2011
18:0
Further
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Click here for quick links to
Annual Reviews content online,
including:
• Other articles in this volume
• Top cited articles
• Top downloaded articles
• Our comprehensive search
Marine Fungi: Their Ecology
and Molecular Diversity
Thomas A. Richards, Meredith D.M. Jones,
Guy Leonard, and David Bass
Department of Zoology, Natural History Museum, London SW7 5BD, United Kingdom;
email: [email protected], [email protected], [email protected], [email protected]
Annu. Rev. Mar. Sci. 2012. 4:495–522
Keywords
First published online as a Review in Advance on
September 19, 2011
saprotroph, osmotroph, parasite, pseudofungi, chytrid, small subunit
ribosomal DNA
The Annual Review of Marine Science is online at
marine.annualreviews.org
This article’s doi:
10.1146/annurev-marine-120710-100802
c 2012 by Annual Reviews.
Copyright All rights reserved
1941-1405/12/0115-0495$20.00
Abstract
Fungi appear to be rare in marine environments. There are relatively few
marine isolates in culture, and fungal small subunit ribosomal DNA (SSU
rDNA) sequences are rarely recovered in marine clone library experiments
(i.e., culture-independent sequence surveys of eukaryotic microbial diversity
from environmental DNA samples). To explore the diversity of marine fungi,
we took a broad selection of SSU rDNA data sets and calculated a summary
phylogeny. Bringing these data together identified a diverse collection of
marine fungi, including sequences branching close to chytrids (flagellated
fungi), filamentous hypha-forming fungi, and multicellular fungi. However,
the majority of the sequences branched with ascomycete and basidiomycete
yeasts. We discuss evidence for 36 novel marine lineages, the majority and
most divergent of which branch with the chytrids. We then investigate what
these data mean for the evolutionary history of the Fungi and specifically
marine-terrestrial transitions. Finally, we discuss the roles of fungi in marine
ecosystems.
495
MA04CH20-Richards
ARI
3 November 2011
18:0
INTRODUCTION
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Fungi are key players in terrestrial environments (Gargas et al. 1995, James et al. 2006a, Wang
& Qiu 2006) and perform vital functions as decomposers, driving nutrient cycles in detritus
environments, and as parasites and symbionts (Webster & Weber 2007). Fungi represent a significant proportion of the microbial diversity on Earth (Hawksworth 2001, Hibbett et al. 2007,
Mueller et al. 2007, O’Brien et al. 2005). The total diversity of the Fungi has been estimated to be
1.5–1.6 million species (Hawksworth 1991, 2001). However, much of our current understanding
of the ecology and evolutionary complexity of fungi is derived from the study of cultured fungal
isolates in the most part from terrestrial environments. Furthermore, this diversity estimate is
based on the study of fungal communities in and around plant ecosystems sampled from Western
Europe and then extrapolated to a global figure using data on global plant diversity (Hawksworth
1991, 2001). This is controversial because it assumes that plant species diversity and fungal species
diversity are correlated (May 1991, 1994; Mueller & Schmit 2007) and is likely to be too low
because it is based on counts derived from morphological observations and therefore does not
account for cryptic species diversity (Hawksworth 2001). Perhaps even more importantly, the estimate focuses only on fungi in a limited set of habitats and therefore does not account for diverse
and abundant fungi that are not associated with plant and soil environments, such as animal hosts,
sediment, freshwater, or marine ecosystems.
Our understanding of fungal evolutionary complexity is expanding as researchers use increasingly powerful molecular methods to investigate environmental diversity (e.g., Buée et al. 2009,
Jumpponen & Jones 2009, O’Brien et al. 2005). For example, work using sequencing of internal transcribed spacer (ITS) markers from soil DNA samples has suggested a revision of global
fungal diversity from Hawksworth’s estimate of 1.5 million species to 3.5–5.1 million (O’Brien
et al. 2005). Yet current culture collections of fungi number only ∼75,000 isolates (Hawksworth
2001, Kis-Papo 2005) with updated counts suggesting 64,000 ascomycete isolates and 32,000 basidiomycete isolates (Kirk et al. 2008), not all of them representing different species. Independent
of the accuracy of these estimates, it is likely that less than 5% of the diversity of fungal species
is currently described and maintained in culture. Furthermore, the use of environmental DNA
(eDNA) methods is increasingly expanding our understanding of the diversity of fungi at the highest taxonomic levels with a number of discoveries of previously undescribed phylogroups ( Jones
et al. 2011, Lara et al. 2010, Porter et al. 2008, Schadt et al. 2003), suggesting that these estimates
are conservative and that culture collections are in no way representative of natural diversity.
Of the cultured species (Hawksworth 2001, Kis-Papo 2005), one count suggests there are only
467 isolates belonging to 244 genera retrieved from marine environments (Kis-Papo 2005). This
might imply that only ∼0.6% of studied fungi are derived from the marine environment, which
would be surprising as marine habitats account for 70% of the surface of the globe and have
been shown to harbor fungi from the air-surface interface to depths of kilometers. These results
have been interpreted to suggest that fungi are both nondiverse and low in abundance in marine
environments (Burgaud et al. 2009, Kis-Papo 2005, Le Calvez et al. 2009). In contrast, fungi
are thought to be a major contributor to the decomposition of woody and herbaceous substrates
and animal remains in coastal and surface marine environments (Kohlmeyer & Kohlmeyer 1979,
Mann 1988, Newell 1996). This raises questions about the significance of fungal communities in
marine environments: Are we overlooking a large diversity of fungi?
The purpose of this review is to bring together the growing body of molecular data, focusing
primarily on environmental small subunit ribosomal DNA (SSU rDNA) sequence data to summarize our current knowledge of the evolutionary diversity of marine fungi. Using these data, we can
begin to investigate a number of theories and observations relating to the ecological role of fungi
496
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
18:0
in marine ecosystems. We hope this will form an important foundation for better understanding
of the diversity and function of fungi in marine environments as metagenomic and large-scale
diversity sequencing projects gather pace.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MOLECULAR DIVERSITY OF MARINE FUNGI
The kingdom Fungi was traditionally loosely classified as four major groups: (a) Ascomycota,
(b) Basidiomycota (which together form the subkingdom Dikarya and have been the major focus
of experimental research and genome-sequencing initiatives), (c) the zygomycetes, and (d ) the
chytrids (Hibbett et al. 2007, Jones et al. 2011, Webster & Weber 2007). This early model of fungal
taxonomy has been revised at a number of levels, including the placement of the microsporidia
with (Hirt et al. 1997, 1999) and potentially within the Fungi (Adl et al. 2005, James et al. 2006a,
Keeling 2003) and the division of the chytrids and zygomycetes into multiple interbranching
paraphyletic clades, followed by subsequent taxonomic reclassifications (see Hibbett et al. 2007;
James et al. 2006a,b; Liu et al. 2009). There still remains much uncertainty relating to the major
divisions of the Fungi below the Dikarya.
Progress in drawing the fungal tree of life has been made by studying fungi that have been isolated and cultured mainly from terrestrial environments (Hibbett et al. 2007; James et al. 2006a,b;
Liu et al. 2009). These approaches are limited because they preferentially sample microbes that
are easily cultured or that possess larger body sizes and/or distinctive morphologies. Furthermore,
these approaches bring their own specific limitations for studying fungi in marine environments:
1. The culturing of fungal isolates from marine samples has often led to the recovery of nonfungal microbes, which are ecologically, morphologically, and trophically similar to fungi
but are not true fungi (discussed below).
2. The ecological preferences of most fungi suggest that those in marine ecosystems are likely
to reside on or in host organisms or in benthic environments, including deep-sea sediments.
These habitats are difficult to examine by microscopy and in some cases pose severe sampling
difficulties.
3. The majority of fungi harbor very high levels of cryptic diversity that is indistinguishable
using microscopy of environmental samples and/or culturing. Further complications arise
because similar fungal morphotypes such as yeasts and flagellated zoospores branch in distant
and paraphyletic positions on the fungal tree of life ( James et al. 2006a, Liu et al. 2009),
making classifications based on observations of general morphological characters difficult
and often misleading.
Molecular methods—specifically the polymerase chain reaction (PCR) amplification of taxonomically informative gene markers from eDNA samples combined with clone library construction, sequencing, and phylogenetic analyses—have demonstrated that microbial diversity is much
more complicated than previously thought (Giovannoni et al. 1990, López-Garcı́a et al. 2001,
Moon-van der Staay et al. 2001, Olsen et al. 1986, Pace 1997). The environmental DNA, PCR,
and clone library approach has been used for both prokaryotes and eukaryotes to place many previously unrecognized branches on the tree of life, in many cases redefining our understanding of the
evolutionary complexity of the eukaryotes (Bass & Cavalier-Smith 2004, Dawson & Pace 2002,
Edgcomb et al. 2002, López-Garcı́a et al. 2001, Moon-van der Staay et al. 2001, Pace 1997, Rappé
& Giovannoni 2003, Richards & Bass 2005, Richards et al. 2005, Stoeck et al. 2006), although
these results have been the subject of much debate and revision (e.g., Berney et al. 2004, CavalierSmith 2004). Molecular approaches have also demonstrated that poorly recognized groups are
important ecosystem components (Bass & Cavalier-Smith 2004, Chambouvet et al. 2008, Massana
et al. 2004b, Moreira & López-Garcia 2002). Yet most molecular surveys of microbial eukaryotic
www.annualreviews.org • Marine Fungi
Ascomycota:
filamentous or yeast
forms that reproduce
sexually with internal
spore maturation
within a sac-shaped
cell called an ascus;
include the laboratory
model organisms
Saccharomyces cerevisiae
and Neurospora crassa
Basidiomycota:
filamentous or yeast
forms that reproduce
sexually with external
spore maturation on a
basidium
Zygomycete:
multinucleated cell
that produces
filaments and lacks a
complex fruiting body
Chytrid: informal
name given to a fungus
that produces motile
flagellated spores
(zoospores) during its
life cycle
True fungi: large and
highly diverse group of
eukaryotes (mainly
microbes, largely
osmotrophic and
frequently with
chitin-rich cell walls)
that form a large clade
in the opisthokont
supergroup
497
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
Small subunit
ribosomal DNA
(SSU rDNA) clone
library: experimental
process involving the
extraction of DNA
from environmental
samples, PCR-targeted
amplification of SSU
rRNA (marker) genes,
cloning of amplicons,
clone sequencing, and
phylogenetic analysis
18:0
diversity are recovered using only one primer set and sample less than 500 clones, with the result
that no eukaryote-wide study has reached sampling saturation (e.g., Edgcomb et al. 2002, Stoeck
et al. 2006). This has led to the suggestion that further sampling from the very same environments
would reveal more diversity and demonstrate that our understanding of the complexity of the tree
of life is still very incomplete (Curtis et al. 2002, Moreira & López-Garcia 2002, Sogin et al. 2006,
Stoeck et al. 2006).
Environmental clone library analyses specifically targeting fungi have generally sampled regions
within the ribosomal RNA (rRNA) gene array using a range of approaches and sequence targets,
with some researchers focusing on the SSU rDNA sequence and others on the ITS regions. The
two ITS regions are sections of DNA located between the SSU (18S) and large subunit (LSU) (28S)
rRNA genes, separated by the 5.8S rRNA gene. The variable nature of the ITS regions relative to
the flanking rRNA genes enables increased resolution and accuracy when assigning sequences to
genus- and species-level classifications within well-sampled groups (Bruns & Gardes 1993, Gardes
& Bruns 1993, Horton & Bruns 2001). This process is facilitated by increasingly well-sampled
sequence databases (Buchan et al. 2002, James et al. 2006a, O’Brien et al. 2005). However, many
database sequence classifications may be erroneous (Vilgalys 2003), and variation in rates of ITS
divergence between taxonomic groups can hinder classifications using these sequences (Nilsson
et al. 2008, 2006; Vilgalys 2003). The ITS approach is useful for determining species diversity and
can be used for ecosystem comparisons when targeting well-defined taxonomic groups, but it is
of limited use for inferring higher-level phylogenetic relationships and identifying novel groups,
as ITS phylogenies demonstrate weak resolution among deeper branching relationships in the
Fungi (Horton & Bruns 2001).
Some researchers have focused on sampling the SSU rRNA gene to investigate novel fungal
diversity among higher taxonomic groups (Anderson et al. 2003, Bass et al. 2007, Jebaraj et al.
2009, Porter et al. 2008, Schadt et al. 2003, Vandenkoornhuyse et al. 2002), although this gene
cannot discriminate between closely related fungal species and is generally less intensively sampled
than the ITS regions. Therefore, others have called for the combination of the SSU and ITS
approaches (O’Brien et al. 2005), enabling multigene phylogenetic analyses encompassing the
SSU, 5.8S, and LSU sequences, which can lead to improved phylogenetic support among both
lower and higher phylogenetic nodes (e.g., Jones et al. 2011, Porter et al. 2008) and help to identify
the phylogenetic placement of many orphan environmental ITS sequences currently accumulating
in sequence databases.
Molecular Sampling in Marine Environments
There is now a growing trend in the use of molecular techniques to investigate microbial diversity
from marine environments. These data have given a mixed impression of the relative importance of
fungal lineages in marine environments. For example, in 2005 we conducted a meta-analysis of 13
SSU rDNA clone library studies. This analysis brought together 49 SSU rDNA environmental
clone libraries, with a total of 1,077 sequences from soils, freshwater, and marine samples. Of
these sequences, 124 (11.5%) clustered within, or close to, known fungal sequences (Richards
& Bass 2005). This analysis also suggested that although fungi are present in aquatic sediments,
low-oxygen aquatic environments, freshwater, and soils, there appeared to be very few sequences
recovered from the upper column and surface marine waters. This pattern was confirmed by a
separate, specifically marine analysis, which sampled 23 coastal water libraries (1,349 clones) and
12 open ocean libraries (826 clones) and recovered a total of only 16 fungal clones, equivalent to
0.8% of the marine SSU rDNA sequences sampled (Massana & Pedrós-Alió 2008). Consequently,
both molecular analyses and culture-based inventories (Kis-Papo 2005) have suggested that fungi
are relatively nondiverse and in low abundance in upper and surface marine ecosystems.
498
Richards et al.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
18:0
Sequencing of eukaryotic SSU rDNA V9 and V4 diversity tags from marine coastal waters using 454 methods has hinted that such environments contain more fungal diversity than previously
detected using clone library methods (Stoeck et al. 2010). These diversity sequencing methods
still suggest that, compared with other eukaryotic groups, fungi appear relatively nondiverse, constituting less than 5% of the operational taxonomic units recovered from marine environments.
However, these methods hint at an increased diversity in comparison with clone library methods
(Pawlowski et al. 2011, Stoeck et al. 2010). Furthermore, fungal-specific clone library analyses have
identified new fungal diversity in deep waters, anoxic marine waters, hydrothermal vent environments, and deep-sea marine sediments (Bass et al. 2007, Burgaud et al. 2009, Edgcomb et al. 2011,
Jebaraj et al. 2009, Le Calvez et al. 2009). The results of this summary and other fungal sequences
detected in marine environments are summarized in Figures 1–5. This work has made use of a
range of eDNA samples and sampling techniques and has therefore made it feasible to sample
previously inaccessible microbial communities, for example, specifically targeting communities in
deep-sea environments.
Deep-Sea and Hydrothermal Vent Environments
Using SSU rDNA clone library methods, Bass and coauthors (2007) investigated the composition
of fungal communities in deep-sea sediments and water column samples of depths of 500 m to
4,200 m, including several hydrothermal vent samples. The sequences recovered showed deepsea fungal communities to be dominated by ascomycete and basidiomycete forms but generally revealed a low diversity of fungi. The authors also noted that the vast majority of these sequences branched closest to taxonomic groups known to have a yeast morphotype, suggesting that
(a) these taxa were easier to recover or (b) yeast forms dominate these environments. Many of these
phylotypes were also shown to branch close to known pathogens, suggesting the presence of fungal
pathogens of deep-sea animals (discussed in detail below). The phylogeny reported by Bass et al.
(2007) included additional marine environmental SSU rDNA sequences recovered from general
eukaryotic PCR experiments and showed seven clusters of highly unique sequences, six of which
branched specifically within the fungal radiation, indicating the presence of unknown fungal forms
in marine environments.
A study by Le Calvez et al. (2009) using similar eDNA methods and targeting deep-sea hydrothermal vent ecosystems also recovered several novel fungal lineages. These lineages included
three unknown phylotypes branching within the basidiomycete radiation and two unknown phylotypes branching close to chytrid sequences (Le Calvez et al. 2009). The primer set used in
this study was different from that chosen by Bass et al. (2007), but both studies demonstrate the
identification of novel fungal lineages in deep-sea marine environments.
Edgcomb et al. (2011) again used similar approaches to identify eukaryotic microbial communities in deep-sea sediment cores but this time targeted both DNA- and RNA-based diversity
profiles. Although the authors specifically targeted a wide diversity of eukaryotic microbes, they
consistently recovered a high frequency of basidiomycete yeast sequences branching closely to
known Cryptococcus and Malassezia species (Edgcomb et al. 2011): 42% of the sequences recovered
from RNA-derived libraries branched with Cryptococcus sequences. This result is consistent with
another molecular analysis of eukaryotic diversity in marine sediments showing that Cryptococcus
curvatus yeasts, with a closely related genotype to those recovered by Edgcomb et al. (2011), can
dominate deep-sea microbial eukaryotic communities (Takishita et al. 2006), whereas culture sampling has recovered a related Cryptococcus species (Cryptococcus surugensis) from deep-sea sediments
(Nagahama et al. 2003b) (shown in Figure 3). The recovery of these taxa in RNA-derived libraries
suggests that they are metabolically active in sedimentary ecosystems (Edgcomb et al. 2011).
www.annualreviews.org • Marine Fungi
499
MA04CH20-Richards
ARI
3 November 2011
Saprotrophy: process
of acquiring nutrients
from the digestion of
dead organic matter,
usually from plants or
animals
18:0
Interestingly, the vast majority of the fungi sampled from deep-sea environments branch close
to, or within, clades of known terrestrial fungi. This suggests that in many cases fungi residing in
terrestrial or marine surface environments are capable of relatively easily making the transition
to deep-sea habitats and is consistent with evidence that some fungi are capable of altering their
membrane composition to tolerate high hydrostatic pressure under short-term experimental conditions (Simonato et al. 2006). Taken together, these data imply that for some fungi, colonization
of deep-sea habitats by surface-dwelling strains is a viable ecological transition.
Anoxic Marine Environments
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
A large fraction of the marine biosphere is anoxic or partially anoxic. In terrestrial environments,
fungi are regularly found in saprotrophic and detritus habitats that are often low in oxygen.
Fungi have been shown to possess a range of cellular and genomic adaptations to life in anoxic
environments (e.g., Embley 2006, Gojkovic et al. 2004, Hall et al. 2005). Furthermore, many fungi
have been shown to play a role in anaerobic denitrification (Shoun et al. 1992), e.g., Fusarium
oxyporum (Takaya et al. 1999, Uchimura et al. 2002). SSU rDNA sequences closely related to
F. oxyporum have been recovered from marine anaerobic environments (Figure 1; Jebaraj et al.
2009), and four marine isolates, including a Fusarium species, have been demonstrated to grow
in suboxic conditions, utilizing nitrate for respiration and accumulating nitrite, and are therefore
theoretically capable of participating in anaerobic denitrification in marine environments ( Jebaraj
& Raghukumar 2009).
A study by Jebaraj et al. (2009) examined the diversity of fungi in oxygen-depleted regions
of the Arabian Sea using clone library methods. These researchers used multiple fungal-specific
SSU rDNA primer sets and one general eukaryotic-specific primer set to amplify SSU sequences
( Jebaraj et al. 2009). Each primer set revealed an overlapping subset of fungal diversity, with
the fungal-specific primers showing a greater diversity of fungi per sampling effort than clone
libraries constructed using universal eukaryotic primers. This result demonstrates the importance
of using different primers to control for PCR biases and suggests that a significant portion of
fungal diversity is missed when using universal primer sets ( Jebaraj et al. 2009, Stoeck et al. 2006).
The phylogeny of Jebaraj et al. (2009) identified 48 distinct fungal phylotypes (clustered at
99% sequence similarity): 27 branching within the ascomycete radiation, 20 branching within the
basidiomycetes, and only 1 unique phylotype branching among the lower fungi. Several Dikarya
sequences formed highly novel branching positions in the phylogeny and clustered with additional
environmental sequences recovered from oxygen-depleted habitats ( Jebaraj et al. 2009). Indeed,
many sequences branched within a clade previously termed the hydrothermal and/or anaerobic
fungal group, which branches with the Malassezia yeasts also identified from deep-sea eukaryotic
environmental clone libraries (Bass et al. 2007, Edgcomb et al. 2011, López-Garcia et al. 2007)—
this interesting group is discussed further below. No chytrid-like sequences were identified from
this study, suggesting the possibility that these taxonomic groups have a low diversity in the marine
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 1
Subsection of a phylogenetic analysis showing the diversity of small subunit ribosomal DNA sequences recovered from marine
environmental DNA analyses. This section of the tree focuses on Pezizomycotina. The tree was calculated using PhyML (parameters
= 0.722 and I = 0.117) with both PhyML and LogDet distance bootstraps. Marine phylotypes are highlighted in yellow. Novel
marine phylogenetic groups are marked NMFA (red, novel marine fungi ascomycetes). Gray dashed lines are false branch extensions.
Ecological information is annotated on the tree.
500
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
18:0
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Isolate: FCAS123 [GQ120177.1]
eDNA: GoC5_E11 [FJ153721.1]
Isolate: Mo7 [EU887758.1]
eDNA: UI12H09 [EU446322.1]
Fungal agent of coral
disease (Alker et al. 2001)
Aspergillus sydowii [EU278600.1]
Aspergillus fumigatus [M60300.1]
eDNA: LL2_BASS [EU154986.1]
Isolate: FCAS50 [GQ120176.1]
Marine fungus
eDNA: A1_E044 [AY046710.1]
eDNA: FAS_19 [GQ120115.1]
>79% bootstrap support
eDNA: FAS_21 [GQ120118.1]
>49% bootstrap support
Penicillium verruculosum [AF510496.1]
eDNA: FAS_20 [GQ120117.1]
eDNA: BOLA831 [AF372705.1]
0.07
eDNA: BOLA676 [AF372704.1]
eDNA: FAS_18 [GQ120114.1]
eDNA: FAS_42 [GQ120141.1] NMFA1
Isolate: FCAS21 [GQ120162.1]
Chaetosartorya cremea [AB008399.1]
Isolate: MV13 [EU887738.1]
Penicillium chrysogenum [HQ882177.1]
Paecilomyces hepiali [HM135172.1]
eDNA: AT2−4 [AF530541.1]
Isolate:
MV_25C [EF638701.1]
eDNA: UI11B04 [EU446318.1]
Isolate: MV_19C [EF638698.1]
eDNA: [AF290082.2]
Cordyceps sinensis [AB067701.1]
eDNA: FAS_16 [GQ120112.1]
Isolate: FCAS54 [GQ120165.1]
eDNA: FAS_17 [GQ120113.1]
Geosmithia putterillii [AB031390.1]
Isolate: FCAS85 [GQ120166.1]
Isolate: FCAS132 [GQ120160.1]
eDNA: TAGIRI-22 [AB191430.1]
Tritirachium sp. [AB109761.1]
Ajellomyces capsulatus [X58572.1]
Isolate: FCAS30 [GQ120163.1]
Blastomyces dermatitidis [M55624.1]
Microascus cirrosus [M89994.1]
Lacazia loboi [AF255331.1]
Pseudallescheria boydii [U43913.1]
Coccidiodes immitis [M55627.1]
Remispora maritima [HQ111002.1]
Isolate: FCAS40 [GQ120179.1]
Fungal agent of epizootic
Corollospora maritima [U46871.1]
Epicoccum nigrum [AJ295235.1] in mussels at a deep-sea
Isolate: FCAS20 [GQ120173.1]
hydrothermal vent (Van
Isolate: MV_26C [EF638702.1]
Beauveria felina [AY261368.1]
Dover et al. 2001)
Isolate: He5C [EF638691.1]
Stilbocrea macrostoma [AY489693.1]
eDNA: C8 [FN263263.1]
Isolate: FCAS129 [GQ120159.1]
Exophiala sp. [AJ232954.1]
Simplicillium lamellicola [AB214656.1]
Rhinocladiella atrovirens [AJ232937.1]
eDNA: FAS_7 [GQ120151.1]
Nadsoniella nigra [X80706.1]
Isolate: FCASAn−2 [GQ120172.1]
eDNA: Herpotrichiellaceae [DQ314803.1]
eDNA: FAS_8 [GQ120152.1]
Capronia pulcherrima [AJ232944.1]
eDNA: FAS_12 [GQ120108.1]
Heteroconium chaetospira [DQ521604.1]
eDNA: FAS_6 [GQ120150.1]
Isolate: Mo13 [EU887764.1]
Fusarium oxysporum [AB110910.1]
Isolate: GMG_C6 [FJ439580.2]
Fusarium solani [AB473810]
Isolate: MV_1C [EF638692.1]
Isolate: Ex7 [EU887749.1]
Model fungus for
Rhinocladiella phaeophora [AJ232950.1]
eDNA: FAS_11 [GQ120107.1]
studying fungal
Capronia epimyces [AJ232938.1]
Hypocrea jecorina [AF548103.1]
denitrification
Isolate: FCAS31 [GQ120170.1]
eDNA: A1_E031 [AY046698.1]
under low-oxygen
eDNA: FAS_13 [GQ120109.1]
eDNA: FAS_22 [GQ120119.1]
conditions (e.g.,
eDNA:
FAS_14
[GQ120110.1]
eDNA: FAS_23 [GQ120120.1]
Takaya et al. 1999)
Verticillium insectorum [AB214655]
Cladosporium uredinicola [AY251097.2]
Paecilomyces fumosoroseus [AB086629]
Isolate: Mo8 [EU887759.1]
eDNA: UI11F12 [EU446307.1]
Isolate: FCAS122 [GQ120156.1]
Humicola fuscoatra [AY706333.1]
Ramularia grevilleana [GU214578.1]
Neurospora crassa [FJ360521]
Isolate: He2C [EF638689.1]
eDNA: A2_E003 [AY046715.1]
eDNA: FAS_24 [GQ120121.1]
Isolate: HE7 [EU887730.1]
eDNA: LEMD047 [AF372706.1]
Isolate: Mo9 [EU887760.1]
eDNA: 1_5F_92D12b1ab1 [GU972324.1]
eDNA: MV_FS1C [EF638704.1]
eDNA: 1_5F_90B12b1ab1 [GU972322.1]
Coniochaeta velutina [GQ154626.1]
Isolate: Ex3 [EU887745.1]
Sporothrix schenckii [M85053.1]
Arthrinium sacchari [AB220206.1]
eDNA: T41A11 [AY882532.1]
eDNA: He3C [EF638690.1]
Lindra marinera [AY879000.1]
Isolate: DIVA1 [EU887731.1]
Lindra thalassiae [DQ470994.1]
Helicodendron paradoxum [AY856945.1]
Nigrospora oryzae [AB220233.1]
Bulgaria inquinans [EU107260.1]
Physalospora scirpi [AB220204.1]
Hyaloscypha vitreola [EU940080.1]
Isolate: MV14 [EU887739.1]
eDNA: MV_FS3C [EF638705.1]
eDNA: FAS_25 [GQ120122.1]
eDNA: GoC5_A12 [FJ153712.1]
Westerdykella dispersa [U42488.1]
Isolate: Mo2 [EU887753.1]
eDNA: FAS_27 [GQ120124.1]
eDNA: D4P07C06 [EF100327.1]
eDNA: FAS_26 [GQ120123.1]
Aureobasidium pullulans [DQ278883.1]
Isolate: FCAS9 [GQ120158.1]
eDNA: LC23_4EP_18 [DQ504331.1]
Isolate: FCAS44 [GQ120155.1]
eDNA: D3P05F07 [EF100306.1]
Preussia terricola [NG_013151.1]
eDNA: D5P09D06 [EF100360.1]
Lineolata rhizophorae [GU479758]
eDNA: NB13_BASS [EU154991.1]
Dendryphiella salina [EU848586.1]
Isolate: Mo5 [EU887756.1]
Julella avicenniae [AF441175]
Geomyces destructans [GU999983.1]
Herpotrichia juniperi [U42483.1]
eDNA: D2P04H12 [EF100257.1]
Ascocratera manglicola [GU296136]
Aigialus grandis [AF441172]
eDNA: He1C [EF638687.1] NMFA2
Sigmoidea prolifera [DQ104807.1]
Dothideomycetes associated
Helicoon fuscosporum [AY856946.1]
with mangrove wood (Suetrong
Isolate: Mo19 [EU887770.1]
et al. 2009)
Scolecobasidium sp. [FJ439579.2]
Troposporella fumosa [AY856953.1]
Helicascus nypae [GU479755]
Massarina velataspora [GQ925841]
Massarina thalassiae [GQ925843]
Falciformispora lignatilis [GU371835]
eDNA: p15D12 [AY882537.1]
Bipolaris sorokiniana [DQ337383.1]
eDNA: 1_5F_89A12b1ab1 [GU972321.1] NMFA3
Figures 2–5
www.annualreviews.org • Marine Fungi
501
MA04CH20-Richards
ARI
3 November 2011
18:0
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
eDNA: S08H02 [AB468676.1]
eDNA: CYSGM-19 [AB275102.1]
eDNA: KD10_BASS [EU154983.1]
Metschnikoiwa sp. [FJ763557.1]
eDNA: S04H05 [AB468634.1]
eDNA: S04H01 [AB468630.1]
Metschnikoia zobellii [AB023468.1]
eDNA: D4P07A09 [EF100386.1]
Candida agrestis [AB023471.1]
eDNA: D1P02G03 [EF100222.1]
Candida akabanensis [AB013514.1]
eDNA: FAS_43 [GQ120142.1]
eDNA: FAS_1 [GQ120105.1]
eDNA: FAS_2 [GQ120116.1]
Kodamaea ohmeri [GU597327]
Saccharomyces cerevisiae [Z75578]
eDNA: LL7_BASS [EU154987.1]
Kluyveromyces nonfermentans [AB011507.1]
Pichia lachancei [EF550451.1]
eDNA: JJ15_BASS [EU154982.1]
Pichia fermentans [GQ458040.1]
eDNA: D5P09B03 [EF100409.1]
Candida abiesophila [EF550350.1]
eDNA: FAS_4 [GQ120138.1]
eDNA: FAS_3 [GQ120127.1]
Debaromyces hanseii [DQ534402.1]
eDNA: MH1_BASS [EU154990.1]
Candida parapsilosis [GQ395609]
eDNA: FAS_5 [GQ120149.1]
Schizosaccharomyces pombe [X54866]
Taphrina deformans [AJ495826.1]
eDNA: GoC5_E06 [FJ153719.1]
Figure 1
Figures 3–5
Marine fungus
>79% bootstrap support
>49% bootstrap support
0.07
Figure 2
Subsection of a phylogenetic analysis showing the diversity of small subunit ribosomal DNA sequences recovered from marine
environmental DNA analyses. This section of the tree mainly focuses on Saccharomycotina. The tree was calculated using PhyML
(parameters = 0.722 and I = 0.117) with both PhyML and LogDet distance bootstraps. Marine phylotypes are highlighted in yellow.
environments investigated or alternatively that the PCR primers or DNA sampling methodologies
used for this study were collectively biased toward the Dikarya.
Fungal-specific clone library analyses of deeper water column samples, sediments, and anoxic
environments (Bass et al. 2007, Jebaraj et al. 2009, Le Calvez et al. 2009) have significantly increased
the diversity of the fungi recovered from marine studies, especially when compared with surface
water samples (Massana & Pedrós-Alió 2008). Two of these studies ( Jebaraj et al. 2009, Le Calvez
et al. 2009) combined eDNA analysis with isolation and culture experiments, demonstrating little
overlap between the sequences recovered from isolated cultures and eDNA and suggesting the
possible presence of a more complex fungal community than identified either by eDNA or culturebased analyses alone. Nonetheless, marine fungal-specific clone library analyses (Bass et al. 2007,
Edgcomb et al. 2011, Jebaraj et al. 2009, Le Calvez et al. 2009) reveal a simple fungal community
with relatively few phylotypes in total. This is a stark contrast to terrestrial environments, where
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 3
Subsection of a phylogenetic analysis showing the diversity of small subunit ribosomal DNA sequences recovered from marine
environmental DNA analyses. This section of the tree mainly focuses on part of the basidiomycete radiation (see Figure 4 for the
remaining basidiomycete branches). The tree was calculated using PhyML (parameters = 0.722 and I = 0.117) with both PhyML
and LogDet distance bootstraps. Marine phylotypes are highlighted in yellow. Novel marine phylogenetic groups are marked NMFB
(blue, novel marine fungi basidiomycetes). Ecological information is annotated on the tree.
502
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
Marine fungus
>79% bootstrap support
>49% bootstrap support
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
0.07
18:0
eDNA: 10_1F_26b1ab1 [GU972474.1]
eDNA: 10132 [GU972195.1]
NMFB1
eDNA: 10180 [GU972227.1]
eDNA: 10_1F_63b1ab1 [GU972505.1]
eDNA: 1H3cG10 [GU972030.1]
eDNA: 1H3cD8 [GU972011.1]
eDNA: AB3F14RJ10F01 [GU823324.1]
eDNA: 10194 [GU972235.1]
eDNA: PAT6_EK5_11 [DQ504360.1]
eDNA: KM10_BASS [EU154984.1]
eDNA: AT9−6 [AF530542.1]
eDNA: 10109 [GU972179.1]
eDNA: [FN690504.1]
eDNA: RU12192007A11 [HQ427485.1]
eDNA: [FN690505.1]
eDNA: UI14F08 [EU446360.1]
Malassezia restricta [EU192367.1]
eDNA: FAS_41 [GQ120140.1]
eDNA: LC23_5EP_14 [DQ504335.1]
eDNA: BAQA52 [AF372708.1]
eDNA: FAS_40 [GQ120139.1]
eDNA: MV5E1_EF15 [EF638647.1]
eDNA: A93F14RM1E05 [GU823227.1]
eDNA: 5H2dA11 [GU972109.1]
eDNA: CK2_BASS [EU154972.1]
eDNA: MV5E1_EF2 [EF638638.1]
eDNA: FAS_15 [GQ120111.1]
eDNA: BOLA39 [AF372707.1] NMFB2
eDNA: 10137 [GU972199.1] NMFB3
eDNA: 10158 [GU972212.1]
Malassezia furfur [AY083223.1]
eDNA: 1H3dC09 [GU971936.1]
eDNA: BOH3_EK2_20 [DQ504358.1]
eDNA: 1H3dB07 [GU971924.1]
eDNA: 9_1F_90B12b1ab1 [GU972448.1]
eDNA: CE2_BASS [EU154971.1]
Malassezia sympodialis [EU192369.1]
Malassezia pachydermatis [EU192366.1]
Malassezia globosa [EU192364.1]
eDNA: 10_1F_31b1ab1 [GU972479.1]
eDNA: 10148 [GU972207.1]
NMFB4
eDNA: 10_1F_19b1ab1 [GU972468.1]
Ustilago maydis [X62396]
Isolate: FCAS87 [GQ120167.1]
eDNA: FAS_37 [GQ120135.1]
Moesziomyces bullatus [DQ363307]
eDNA: FAS_38 [GQ120136.1] NMFB5
eDNA: FAS_39 [GQ120137.1]
Thecaphora spilanthis [DQ832242]
eDNA: FAS_51 [GU072550.1]
eDNA: FAS_30 [GQ120128.1]
Isolate: FCAS90 [GQ120171.1]
Graphiola cylindrica [D63929.1]
eDNA: UI12B09 [EU446331.1]
eDNA: cLA11E07 [EU446368.1]
eDNA: LKM33[AJ130854.1]
Exobasidium rhododendri [AJ271381.1]
Doassansia hygrophilae [DQ198788]
Rhamphospora nymphaeae [DQ831033.1]
Tilletiopsis ashingtonensis [AJ271382.1]
Isolate: HE6 [EU887729.1]
Tilletiopsis derxii [AB045704]
eDNA: FAS_33 [GQ120131.1] NMFB6
eDNA: FAS_44 [GQ120143.1]
NMFB7
eDNA: FAS_45 [GQ120144.1]
eDNA: UI13D02 [EU446343.1]
Coprinus cinereus [M92991]
Exidia uvapsassa [NG_013159.1]
eDNA: MV5E1_EF3 [EF638639.1]
Athelia epiphylla [GU187613.1]
eDNA: MV5E1_EF5 [EF638641.1]
Form multicellular bodies
eDNA: FAS_48 [GQ120147.1]
in terrestrial environments
eDNA: FAS_46 [GQ120145.1]
eDNA: FAS_47 [GQ120146.1]
eDNA: NB16_BASS [EU158830.1]
eDNA: JJ14_BASS [EU154981.1]
Antrodia variiformis [AY336782.1]
Cystofilobasidium infirmo-miniatum [AB072226.1]
eDNA: MD13_BASS [EU154988.1]
eDNA: 1H2cA11 [GU971833.1]
eDNA: 1H2cG5 [GU971887.1]
Cryptococcus pseudolongus [AB051047.1]
eDNA: 1H2cD8_1 [GU971902.1]
eDNA: 1H2cD6 [GU971865.1] NMFB8
eDNA: 1H2cA7 [GU971897.1]
Trichosporon aquatile [AB001730]
Dominant microbial eukaryote in sediment at the Kuroshima
eDNA: DSGM-62 [AB275062.1]
Knoll methane seep (Takishita et al. 2006)
eDNA: KUROS1 [AB234889.1]
Cryptococcus curvatus [AB032626]
Cryptococcus surugaensis [AB100440.1]
Yeast species isolated from deep-sea floor sediment,
eDNA: BL00122143 [AY426889.1]
Suruga Bay, Japan (Nagahama et al. 2003b)
eDNA: CH1_S1_56 [AY821990.1]
eDNA: HC8_BASS [EU154978.1]
Cryptococcus carnescens [AB105437.1]
Cryptococcus gattii [HQ659559]
Filobasidium elegans [AB075545.1]
eDNA: H18E12_5 [EF638517.1]
Filobasidium elegans [AB075545.1]
eDNA:[AB505508.1]
eDNA: JJ12_BASS [EU154980.1]
Cryptococcus albidus [HQ231895]
eDNA: MV2E1_40 [EF638491.1] NMFB9
eDNA: MV2E1_7 [EF638470.1]
Figure 4
Figures 1, 2, and 5
www.annualreviews.org • Marine Fungi
503
MA04CH20-Richards
ARI
3 November 2011
18:0
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
eDNA: UI11B06 [EU446299.1]
eDNA: JJ11_BASS [EU154979.1]
eDNA: B42 [FJ914435.1]
Red yeasts isolated from
Rhodotorula glutinis [DQ832194.1]
deep-sea sediments,
eDNA: MD7_BASS [EU154989.1]
Pacific Ocean
eDNA: UI12D05 [EU446334.1]
(Nagahama et al. 2001)
Rhodotorula mucilaginosa [GQ433375.1]
eDNA: FAS_29 [GQ120126.1]
Isolate: FCAS88 [GQ120168.1]
Example of red yeast isolated from
eDNA: FAS_28 [GQ120125.1]
a deep-sea tubeworm, Pacific Ocean
Rhodotorula benthica [AB126647.1]
(Nagahama et al. 2003a)
Rhodotorula nymphaeae [AB055189.1]
Rhodotorula aurantiaca [AB030354.1]
Kurtzmanomyces nectairei [D64122.1]
Sporobolomyces xanthus [D64118.1]
Sporobolomyces pyrrosiae [AB126045.2]
Bensingtonia naganoensis [D38366.1]
eDNA: GoC4_A07 [FJ153692.1]
Kondoa malvinella [D13776.1]
Mycogloea macrospora [U41848.1]
Tritirachium egenum [JF263567.1]
Isolate: FCAS11 [GQ120154.1]
Platygloea disciformis [DQ234563.1]
Figure 3
Figures 1, 2, and 5
Marine fungus
>79% bootstrap support
>49% bootstrap support
0.07
Figure 4
Subsection of a phylogenetic analysis demonstrating the diversity of small subunit ribosomal (SSU) DNA
sequences recovered from marine environmental DNA analyses. This section of the tree focuses on the other
subsection of the basidiomycete phylogeny (see Figure 3 for the remaining basidiomycete branches). The
tree was calculated using PhyML (parameters = 0.722 and I = 0.117) with both PhyML and LogDet
distance bootstraps. Marine phylotypes are highlighted in yellow. Ecological information is annotated on the
tree. Three Rhodotorula sequences are not highlighted in yellow, because actual SSU sequences were not
recovered from a marine environment; marine provenance here is based on comparison of internal
transcribed spacer (ITS) sequences in the papers referenced.
fungal communities appear to be much more complex (e.g., Buée et al. 2009, Jumpponen &
Jones 2009, O’Brien et al. 2005), clearly demonstrated by the comparison of species accumulation
curves from marine environments (Bass et al. 2007, Jebaraj et al. 2009) with the results of clone
library analyses of nonmarine habitats. Based on currently available data, it is difficult to describe
the difference in the diversity and relative abundance of fungal forms between terrestrial and
marine environments. Yet the molecular data seem to be consistent with the results of culturing
efforts, although different diversity profiles are revealed by these two methods, and suggest that
marine fungi are relatively nondiverse and lower in abundance. Therefore, some fundamental
questions remain to be addressed: (a) Is this apparent difference in diversity and abundance due
to an asymmetric sampling effort between marine and terrestrial environments? (b) Is there a
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 5
Subsection of a phylogenetic analysis showing the diversity of small subunit ribosomal DNA sequences recovered from marine
environmental DNA analyses. This section of the tree mainly focuses on the lower fungi (i.e., chytrids and zygomycetes). The tree was
calculated using PhyML (parameters = 0.722 and I = 0.117) with both PhyML and LogDet distance bootstraps. Marine phylotypes
are highlighted in yellow. Novel marine phylogenetic groups are marked NMF (orange, novel marine fungi). Ecological information is
annotated on the tree.
504
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
18:0
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Figures 1–4
Rhopalomyces elegans [NG_017191.1]
eDNA: D1P01D10 [EF100208.1] NMF1
Syncephalis depressa [AB016011.1]
Thamnocephalis sphaerospora [AB016013.1]
Scutellospora dipurpurescens [FM212931.1]
Glomus mosseae [NG_017178]
Paraglomus occultum [NG_017179]
Endogone lactiflua [DQ536471.1]
Marine fungus
eDNA: D5P09E04 [EF100388.1]
eDNA: KD12_BASS [EU154985.1] NMF2
>79% bootstrap support
Chytridiales sp. AF011 [EF432819.2]
>49% bootstrap support
eDNA: NPK97_82 [EU371354.1] NMF3
eDNA: T37A10 [AY882534.1]
eDNA: p15H03 [AY882540.2] NMF4
0.07
eDNA: CCW64 [AY180029.1]
Chytridiales sp. [EF443138]
Lobulomyces angularis [AF164253.2]
Chytriomyces poculatus [EF443135.1]
eDNA:MV5E2_90 [EF638685.1]
eDNA: MV2E2_B7R [EF638571.1] NMF5
eDNA: D2P03H04 [EF100399.1] NMF6
Chytridium polysiphoniae [AY032608.1]
Parasite of brown
eDNA: D2P03H05 [EF100242.1] NMF7
macroalgae
Nowakowskiella sp. [AY635835]
Cladochytrium replicatum [NG_017169]
(Küpper et al. 2006)
Neocallimastix frontalis [EF014370.1]
Piromyces sp. [HQ585899]
Cyllamyces aberensis [DQ536481.1]
Triparticalcar arcticum [DQ536480.1]
Entophlyctis confervae-glomeratae [EF014367.1]
Catenomyces sp. [AY635830.1]
eDNA: DB39_BASS [EU154976.1]
eDNA: AI3F14RJ1H10 [GU823836] NMF8
Entophlyctis sp. [AY635824.1]
eDNA: PA2009A3 [HQ191313.1]
eDNA:T5P2AeD02 [GQ995333.1]
Rhizophlyctis rosea [NG_017175.1]
Basidiobolus ranarum [NG_017184]
Basidiobolus haptosporus [AF368504.1]
Rhizophydium sphaerotheca [AY635823]
Batrachochytrium dendrobatidis (Broad genome project)
eDNA: D3P06C06 [EF100403.1] NMF9
Kappamyces laurelensis [DQ536478.1]
Rhizophydium sp. [AY635821.1]
eDNA: T5P2AeG04 [GQ995437.1] NMF10
eDNA: BAQA128 [AF372721.1] NMF11
eDNA: BL01032036 [AY426915.1] NMF12
Rhizophlyctis harderi [AF164272.2]
Rhizophydium elyensis [DQ536479.1]
eDNA: M1_18C05 [DQ103818.1] NMF13
Rhizophydium sp. [DQ536492.1]
Karlingiomyces sp. [AF164278]
Polychytrium aggregatum [NG_017168]
Mortierella olfii [AF113425.1]
Mortierella chlamydospora [AF157143.1]
Blastocladiella emersonii [AY635842]
Allomyces arbuscula [NG_017166]
eDNA: TAGIRI-24 [AB191432.1] NMF14
Rhizoclosmatium sp. [AY601709.1]
Chytriomyces hyalinus [DQ536487]
Hyaloraphidium curvatum [NG_017172]
Monoblepharella sp. [AY546682]
eDNA: I34 [EU910604]
eDNA: BAQA64 [AF372718.1] NMF15
eDNA: LKM15 [AJ130850]
eDNA: IAFDv7 [AY835675.2] NMF16
eDNA: NAMAKO-36 AB252776
Rozella sp. [AY601707]
Rozella allomycis [AY635838]
eDNA: DSGM-64 [AB275064.1]
NMF17
eDNA: TAGIRI-23 [AB191431.1]
eDNA: NAMAKO-37 [AB252777]
eDNA: NAMAKO-35 [AB252775.1]
eDNA: CCW48 [AY180024.1] NMF18
eDNA: CCW24 [AY230211.1] NMF19
eDNA: LKM46 [AJ130857]
eDNA: BL01032033 [AY426912.1] NMF20
eDNA: EMPE7 [AF372715.1]
eDNA: LS_CM2 [FJ687267.1]
eDNA: BRKC111 [AF372714.1]
eDNA: GoC6_F01 [FJ153737.1] NMF21
eDNA: WS_CM1 [FJ687268]
eDNA: IAFDv110 [AY835696.2] NMF22
eDNA: LKM11: [AJ130849]
Cryptomycota
eDNA: BAQA254 [AF372713.1]
(Jones et al. 2011)
eDNA: BAQA04 [AF372712.1] NMF23
eDNA: KD14_BASS [EU154992.1]
eDNA: [AB468638.1]
eDNA: [AB275063.1]
NMF24
eDNA: SS1_E_01_42 [EU050974.1]
eDNA: SS1_E_01_10 [EU050973.1]
Physoderma dulichii [DQ536472]
Physoderma maculare [DQ536489]
Amoebidium parasiticum [Y19155]
eDNA: NW61702 [DQ060525.1]
eDNA: FAS_49 [GQ120148.1]
Outgroup
Nuclearia simplex
Capsaspora owczarzaki
Suberites ficus [AJ627184]
Aurelia sp. [EU276014]
www.annualreviews.org • Marine Fungi
505
MA04CH20-Richards
ARI
3 November 2011
18:0
real ecological barrier that has prevented marine fungi from diversifying to the same degree as
terrestrial fungi? (c) Is the broad success and evolutionary complexity of the fungal radiation so
intimately linked with the radiation of land plants and the colonization of terrestrial environments
that these forms dominate the diversity of the fungal kingdom? (d ) Are marine niches dominated
by a different set of microbes performing the equivalent roles in the ecosystem as fungi in terrestrial
environments, so as to outcompete fungi in marine habitats? To begin to address these questions,
it is important to investigate which fungi have been detected in marine environments.
PHYLOGENETIC SUMMARY OF THE SMALL SUBUNIT RIBOSOMAL
DNA DIVERSITY OF MARINE FUNGI
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
To bring together the growing body of data investigating the molecular diversity of fungi in
marine environments, we have calculated a summary phylogenetic tree of all unique fungal SSU
rDNA sequences detected from marine eDNA samples. Sampling was conducted by a literature
review followed by phylogenetic tree construction to obtain a preliminary census of the molecular
diversity of fungal SSU sequences. Using this preliminary tree, we conducted BLASTn searches
(Altschul et al. 1990) of the NCBI nonredundant DNA database (GenBank) to identify additional
marine fungal eDNA SSU sequences. We focused on SSU, rather than ITS, sequences to generate
as robust a phylogeny as possible, allowing us to construct a comprehensive picture of the diversity
and identify any novel or distinct phylogenetic groups. Therefore, many marine culture-derived
sequences are not included in our analysis, as ITS rDNA is often the marker of choice in culturebased studies (Horton & Bruns 2001).
Our tree (Figures 1–5) was constructed in an iterative fashion with many highly similar sequences from the same environment sample and/or publication removed and thus represents a
summary of the diversity of marine fungal SSU sequences available in GenBank. Therefore, this
phylogenetic tree should be viewed not as an exhaustive census, but rather as a summary of our
understanding of the molecular diversity of marine fungi.
We also note that the nucleic acid extraction methods used in many of the published environmental clone library studies often do not include chemical/physical preparations specifically
tailored to the lysis of fungal cells. It is therefore possible that DNA from cells enclosed within
robust chitin-rich cell walls typical of many fungi may have been missed by these studies. Furthermore, the PCR primers used convey differential PCR bias toward or against particular fungal
groups. Therefore, our summary tree is likely to be incomplete and is affected by systematic biases
in the sampling methods used.
The sequences in Figures 1–5 are derived from a range of methods, including both fungalspecific clone library analyses and general eukaryotic analyses, and the sequences used were generated by a number of different primer combinations. Therefore, the number of DNA positions that
could be reliably sampled across all the data sets analyzed was limited. Nonetheless, we were able
to sample a masked alignment region of 656 characters surrounding the variable SSU V4 region
(Wuyts et al. 2000). We then conducted preliminary phylogenetic analysis to remove redundant
and highly similar SSU sequences. The alignment was calculated using MUSCLE (Edgar 2004),
extensively corrected by eye, and was masked using SEAVIEW (Galtier et al. 1996). Phylogenetic
analysis was conducted using PHYML (Guindon & Gascuel 2003) with 100 PHYML bootstraps
and 1,000 LOG-DET distance bootstraps (Lockhart et al. 1994).
The Dikarya Majority on Land and at Sea
Our phylogeny (Figures 1–5) shows a diverse collection of environmental marine fungal SSU
rDNA sequences, with the vast majority branching within the basidiomycetes and ascomycetes
506
Richards et al.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
18:0
(Figures 1–4). This dominance of Dikarya in marine habitats is consistent with previous analyses
(Bass et al. 2007, Edgcomb et al. 2011, Jebaraj et al. 2009, Le Calvez et al. 2009). Many Dikarya
sequences sampled during our preliminary phylogenetic analysis were highly similar to each other;
much of this redundancy was removed during the tree processing steps described above and is
not shown in Figures 1–4. Consequently, this phylogenetic analysis actually underestimates the
relative dominance of Dikarya (Figures 1–4) compared to lower fungi (Figure 5).
Our phylogenetic analysis suggests that filamentous fungi are more diverse in marine habitats
than previous studies have suggested (Bass et al. 2007). Examples include lineages within the
Pezizomycotina ascomycete fungi, Neurospora, Aspergillus, Cordyceps, and Fusarium (Figure 1),
and some basidiomycetes, e.g., Ustilago-like lineages (Figure 3). The phylogeny also identified
several marine sequences branching close to taxa that form multicellular structures in terrestrial
environments, e.g., Coprinus, Antrodia, and Exidia (Figure 3). We had previously suggested that
yeast forms dominate fungal diversity in the deep water column and marine sediment environments
(Bass et al. 2007). The summary phylogeny partially supports this analysis, with a large proportion
of the sequence diversity recovered clustering with known yeast taxa [e.g., Candida, Metschnikowia,
Pichia, Taphrina, Malassezia, Cryptococcus, and Rhodotorula (Figures 2–4)], but suggests that marine
fungal communities comprise a wider diversity of fungal phenotypes.
We also note that a large proportion of the filamentous Pezizomycotina diversity shown in
Figure 1 was recovered from cultured isolates (Burgaud et al. 2009, Jebaraj et al. 2009, Le Calvez
et al. 2009), suggesting that eDNA studies miss these usually filamentous fungi. This may be
explained by primer bias or by the DNA extraction process failing to recover DNA from these
microbes, owing to their robust cell walls reducing DNA recovery from these groups. Alternatively,
these Pezizomycotina microbes may be at a very low level of abundance, or present as cysts, and
are consequently often missed during eDNA sampling. Yet filamentous forms seem to be readily
recovered during culturing experiments, perhaps because this sampling method can preferentially
select for such fungal forms (e.g., Le Calvez et al. 2009). In conclusion, our phylogenetic results
suggest that Dikarya are the most readily recovered marine fungal lineages, and the majority of
sequences recovered from eDNA analyses cluster on the phylogeny with known yeast groups,
although culturing efforts suggest the presence of a higher proportion of filamentous forms.
Novel Marine Fungal Phylotypes and the Marine-Terrestrial Transition
Environmental clone library sequencing has identified a number of novel and phylogenetically
distinct clades that branch with the fungi but seem to represent highly unique groups ( Jones et al.
2011, Lara et al. 2010, Porter et al. 2008, Schadt et al. 2003). Our summary phylogeny shows 36
such groups (Figures 1, 3, and 5). We defined these novel groups on the basis of a minimum
of 3% nucleotide character difference, identified using BLASTn analysis, to all sequences in the
GenBank nonredundant database that were not marine eDNA sequences. Interestingly, although
the majority of marine fungal sequences recovered for this analysis branched within the Dikarya
(Figures 1–4), 24 of the 36 novel groups branched among the lower fungi (Figure 5). Figure 6
plots the percentage difference of all 36 novel fungal groups to cultured and described fungi versus
the percentage difference of the novel groups to all fungal SSU sequences recovered from terrestrial
environments (including both eDNA and cultured isolates). This graph clearly demonstrates that
the novel marine lower fungi generally comprise more divergent SSU types compared to novel
groups within the Dikarya. Furthermore, the novel marine lower fungi seem to be particularly
distantly related to cultured and described fungi. Taken together, these data suggest that marine
environments host a significant number of highly novel groups, with the majority of these novel
groups branching below the Dikarya radiation, close to chytrid branches, implying that they may
www.annualreviews.org • Marine Fungi
507
MA04CH20-Richards
ARI
3 November 2011
18:0
NMF
NMFB (Dikarya)
NMFA (Dikarya)
Line of best fit for novel
marine Dikarya groups
(n = 12, NMFB + NMFA)
Line of best fit for novel
marine lower-fungi groups
(n = 24)
15
14
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Percent difference among SSU sequences from
terrestrial fungi (either cultured isolate or eDNA)
13
12
11
10
9
8
7
6
5
4
3
2
1
0
0
1
2
3
4
5
6
7
8
9
10 11 12 13 14 15 16 17
Percent difference among SSU sequences of all
cultured and described fungal isolates
Figure 6
Graph comparing the percentage difference of novel marine fungi to terrestrial fungi verses the percentage
difference of the novel fungi to all isolated and described fungi (either terrestrial or marine). This graph
demonstrates that among the marine fungi, the novel marine groups branch mainly among the lower fungi
(Figure 5) and that these novel lower fungal branches (shown in orange) have higher levels of small subunit
(SSU) ribosomal DNA sequence difference to cultured and described fungi (x axis) than fungi detected in
terrestrial environments ( y axis). This demonstrates that novel marine fungi (NMF) tend to have closer
relatives detected by sequencing of terrestrial environments than they have represented in culture
collections, suggesting that isolation and description of marine fungi are lagging behind. Abbreviations:
eDNA, environmental DNA; n, number of novel phylotypes identified in the tree analysis (see Figures 1–5);
NMFA, novel marine fungi ascomycetes; NMFB, novel marine fungi basidiomycetes.
form flagellated zoospores (Figure 5). These results are consistent with the conclusion of Le
Calvez et al. (2009), who suggest that the marine environment hosts numerous, unclassified deepbranching fungal forms, reflecting an ancient transition from marine environments to terrestrial
environments. The lower fungi may be significantly more diverse and numerous in marine habitats
than Figure 5 suggests if the PCR process (including primer choice/design) used to generate most
marine clone libraries (whether targeting fungi or microbial eukaryotes in general) is biased toward
Dikarya fungi.
The majority of fungal environmental SSU rDNA sequences and isolated cultures are from
terrestrial environments, leading to the hypothesis that fungi are a mainly terrestrial group (e.g.,
508
Richards et al.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
18:0
Le Calvez et al. 2009). However, all terrestrial life-forms, including freshwater forms, must trace
their ancestry back to marine-dwelling ancestors. It has therefore been inferred that fungi arose
in the oceans and then colonized terrestrial environments (Le Calvez et al. 2009). The transition
from marine to terrestrial environments involves a radical change in biological capacities, and
therefore it is widely suggested that symbioses between fungi and photosynthetic microbes facilitated multiple terrestrial colonization events, including the phototrophic microbial ancestor of
the land plants (Pirozynski & Malloch 1975, Selosse & Le Tacon 1998, Simon et al. 1993). Fossil
evidence has suggested that several fungal subgroups [e.g., vesicular-arbuscular (VA) mycorrhizae,
ascomycetes, blastocladiomycetes] were established in the Devonian 400 Mya, suggesting the fungal lineage is much older than this (Berbee & Taylor 2010) and therefore that the fungal kingdom
is much older than the colonization of land by both plants and fungi. These results imply a long
phase of fungal evolution in aquatic/marine environments before fungi colonized the land (i.e., an
ancient marine fungal divergence) (Le Calvez et al. 2009). Evidence of divergent deep-branching
marine fungal SSU sequences (e.g., Figures 5 and 6) has been used to argue that these lower fungal marine groups are derived from an ancient phase of fungal evolution in marine environments
prior to the colonization of terrestrial environments (Le Calvez et al. 2009). However, environmental sequencing of marine DNA samples also shows that marine lineages frequently form short
branches interdispersed between terrestrial lineages (Figures 1–5). One interpretation is that the
evolutionary diversification of the Fungi has involved multiple marine-terrestrial transitions in
both directions.
In contradiction to the ancient marine fungal divergence theory, studies of freshwater environments have recovered novel deep-branching fungal sequences at a much higher frequency than in
the marine environment. For example, freshwater studies frequently report that a high proportion
of all the clones recovered from general eukaryotic clone libraries are fungal sequences [e.g., 19%
(Lef èvre et al. 2008), 23% (Lef èvre et al. 2007), 33% (Berney et al. 2004), or 25% (Lepère et al.
2006)]. Furthermore, in contrast to the majority of fungal sequences recovered from marine environments, which are Dikarya (e.g., Figures 1–5; Bass et al. 2007, Edgcomb et al. 2011, Jebaraj et al.
2009, Le Calvez et al. 2009), a much larger proportion of the freshwater fungal sequences branch
among the lower fungi (Figure 7). These results point to a large and underexplored diversity of
lower fungal groups in freshwater (Lef èvre et al. 2007, 2008; Lefranc et al. 2005; Slapeta et al.
2005) compared to marine environments. With freshwater environments being part of the terrestrial biome, this emerging pattern therefore seems to be inconsistent with the idea that divergent
deep-branching novel fungal forms are derived directly from marine ancestors, separate from the
terrestrial branch(es) (Le Calvez et al. 2009). A more realistic model might be a terrestrial origin or
very early primary terrestrial radiation of fungi followed by multiple marine-terrestrial transitions
in both directions. Indeed, phylogenetic analysis of marine ascomycetes has identified multiple
terrestrial-to-marine transitions (Spatafora et al. 1998, Suetrong et al. 2009), whereas data supporting multiple losses of flagella within the fungal radiation ( James et al. 2006a,b; Liu et al. 2009) show
a similarly complex evolutionary pattern involving multiple aquatic-to-nonaquatic transitions.
Cryptomycota: A New Basal Branch in the Fungi?
Interestingly, freshwater studies have also identified a large and complex clade of environmental
sequences that form one of the deepest branches in the Fungi (e.g., Berney et al. 2004; Lef èvre
et al. 2007, 2008; van Hannen et al. 1999). Van Hannen and coauthors (1999) first identified this
group from sequencing DNA recovered from a freshwater-derived experimental detritus system,
and it has now been recovered from numerous environment types ( Jones et al. 2011, Lara et al.
2010). Of the four fungal-like sequences recovered by van Hannen et al. (1999), three formed this
www.annualreviews.org • Marine Fungi
509
MA04CH20-Richards
ARI
3 November 2011
18:0
Edgcomb et al. (2011)
deep-sea sediment
with a nested PCR step
Marine fungi identifed using
seven different primer sets
(five fungal specific)
Le Calvez et al. (2009)
hydrothermal vents
Bass et al. (2007)
deep sea
Jebaraj et al. (2009)
oxygen-depleted Arabian
sea environments
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Lefèvre et al. (2008)
lake water
picoeukaryotes 2
Lefèvre et al. (2007)
lake water
picoeukaryotes 1
Freshwater fungi identified
using three different general
eukaryotic primer sets
Lefranc et al. (2005)
lake water columns
Berney et al. (2004)
stream sediment
10
20
30
40
50
Phylotypes
Dikarya
Lower fungi
Figure 7
Comparison of small subunit ribosomal clone library analyses from marine and freshwater environmental
DNAs, demonstrating that freshwater sampling identifies many more lower fungi phylotypes than similar
marine analyses, whereas marine analyses tend to detect Dikarya fungi. Note that the freshwater studies
summarized used general eukaryotic primers, whereas the marine studies summarized used both general
eukaryotic primers and fungal-specific primers.
Phagotrophy:
process of acquiring
nutrients by engulfing
large particles or prey
cells in a phagosome
(cell vacuole), followed
by digestion and
intracellular
absorption of nutrients
Osmotrophy: mode
of nutrition involving
secretion of enzymes
to break down complex
biological polymers
followed by uptake of
simplified molecules
510
deep-branching clade. Subsequent clone library experiments have considerably expanded the diversity of this clade in soils and freshwater environments (e.g., Jones et al. 2011; Lef èvre et al.
2007, 2008; Lefranc et al. 2005); sequencing of marine libraries has also recovered representatives
of this group (Figure 5; also see Massana et al. 2004a; Takishita et al. 2005, 2007). Using terminal
restriction fragment length polymorphism analyses, Lepère et al. (2006) found that representatives
of this group are highly abundant in freshwater environments and that population abundance is
linked to an abundance of algal populations.
Further phylogenetic analysis with additional environmental rDNA sampling suggests that
this group branches with the intracellular parasitic genus Rozella, thought to be the first branch
in the fungal radiation ( James et al. 2006a, Jones et al. 2011, Lara et al. 2010). This is an interesting relationship because the genus Rozella comprises intracellular parasites that do not possess
a chitin/cellulose cell wall for the stages of their life cycle identified and furthermore appear to
be capable of phagotrophy (Held 1981). These characteristics represent distinct differences from
the fundamental fungal phenotype: a rigid chitin wall, the use of osmotrophy, and an inability
to perform phagotrophy. Thus it is questionable whether the Rozella genus and this wider clade
of environmental sequences should be classified within the Fungi or whether they represent an
intermediate form (Lara et al. 2010, Jones et al. 2011).
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
18:0
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Jones et al. (2011) used fluorescence in situ hybridization to investigate the ecology and cell
biology of this novel group and showed that it possesses at least three distinct life-cycle phases:
(a) a flagellated zoospore, (b) single cells attached to other (often algal) cells, and (c) cysts or
resting cells. Using a combination of cell wall markers, the authors could not identify a fungal
chitin/cellulose cell wall, suggesting that similar to Rozella, these microbes live without this cellular
trait for much of their life cycle. In anticipation of formal classification, and because this clade
groups with true fungi, Jones et al. (2011) named this group cryptomycota (hidden fungi).
Interestingly, both the cryptomycota and chytrid-like sequences recovered from freshwater
environments branch most closely to fungi known to parasitize algae, other fungi, or protists (Held
1981; Lef èvre et al. 2007, 2008; Lefranc et al. 2005). These observations have led some authors
to re-evaluate the functional role of fungal parasites in freshwater environments, suggesting that
they play a significant role in the microbial loop of freshwater ecosystems (Lef èvre et al. 2008).
Cryptomycota:
highly diverse group of
microbes, mainly
known from
environmental DNA
techniques; includes
Rozella
ECOLOGICAL ROLE OF FUNGI IN MARINE ENVIRONMENTS
Fungi are considered as saprotrophs, parasites, or symbionts, partly because of the bias of research
interests, but mainly as a consequence of the evolution of fungal cell biology and feeding strategies.
In contrast to the example of the cryptomycota discussed above ( Jones et al. 2011), fungi generally
possess robust chitin-rich cell walls and obtain nutrients exclusively by feeding osmotrophically.
This process involves the secretion of depolymerizing enzymes followed by the transportation of
nutrients, usually as digested monomers, back into the cell.
These traits underpin the ecological success of the Fungi and are mechanistically linked;
the chitin/cellulose reinforces the fungal cell and enables it to resist (a) the substantial osmotic
pressure produced during osmotrophic feeding, (b) structural strains during growth (usually as
polarized cells in the form of hyphae or rhizoids), and (c) the diverse and heterogeneous environments within which fungal filaments grow. These adaptations drive the high metabolic rate,
fast growth, and ecological success of fungi (Bartnicki-Garcia 1987). However, as a consequence
of this lifestyle, many fungi have lost the ability to perform phagocytosis and therefore cannot engulf and digest prey cells in the same way as many other eukaryotes. This reliance on
osmotrophy determines the ecology of fungi: They thrive in nutritionally rich environments
such as plant and animal host organisms, soils, sediments, and detritus environments, where they
can attach to substrates, secrete enzymes, break down complex biological polymers, and take up
nutrients.
These ecological characteristics in part may explain why fungi have been considered both
nondiverse and of low abundance in many upper and surface marine water column samples
(Kis-Papo 2005, Massana & Pedrós-Alió 2008, Richards & Bass 2005). Many pelagic and surface
water environments are often low in nutrients, and the microbial eukaryotic component of the
planktonic food chain is predominately that of free-floating or swimming single-celled organisms
performing primary production and/or phagotrophic grazing. Such environments are unlikely to
favor organisms that feed primarily by attachment to larger physical substrates and osmotrophy,
partly because secreted enzymes and target nutrients are likely to be lost by rapid diffusion in the
liquid environment, but also because of key differences in the relationship between photosynthesis
and biomass accumulation on land and at sea. Fixed carbon on land is largely invested in the
construction of large and complex plant tissues rich in energy and nutrients. These complex
structures are difficult to digest, driving the evolution of the osmotrophic lifestyle, specialized
plant/fungi associations, and the subsequent diversification of fungi. Yet in the open ocean,
primary producers do not extend much beyond the scale of small single-celled organisms (∼3 μm
in diameter) and do not make complex energy- and nutrient-rich structures like land plants.
www.annualreviews.org • Marine Fungi
511
ARI
3 November 2011
18:0
As such, the very niches that favor fungal diversification and osmotrophic feeding on land are
largely absent in the open ocean. Therefore, this trophic relationship is essentially closed off to
the microbial community, with only single-celled primary producers and phagotrophic grazers
supported in the upper oceanic water column.
There are, of course, exceptions to this model: (a) In the lower water column, below the photozone, as particulate matter descends and enters the sediment, logically there must be increased
niche availability for saprotrophs (potentially fungi) driving the principal steps in food webs, which
at these lower depths are born out of detritus processing. Observations that fungi are the dominant
active eukaryotic microbes in these environments are consistent with this hypothesis (Edgcomb
et al. 2011, Takishita et al. 2006). Detrital processing represents a largely understudied area of
marine ecology but represents an important gap in our understanding of how nutrients, including
carbon, are processed. (b) Coastal systems harboring large multicellular algae or mangroves must
provide numerous niches for saprotrophs and endophytes, again providing potential ecosystems
for marine fungi (discussed below). (c) A large fraction of marine fungi must also reside as parasitic
forms in marine animals.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
Fungi as Parasitic Agents in the Marine Environment
It is striking that many fungi that cause or are associated with disease in marine habitats are
closely related in phylogenetic analyses to well-characterized nonmarine taxa. Figures 1–3 show
several examples, with marine sequences branching closely to terrestrial parasitic fungi, e.g.,
Cordyceps/Paecilomyces (Figure 1), Geomyces (Figure 1), Taphrina (Figure 2), Candida (Figure 2),
Malassezia (Figure 3), and Ustilago (Figure 3). Furthermore, fungi are often isolated from marine
animals, suggesting a range of additional and unstudied parasitic associations. For example, new
species of the basidiomycete yeast Rhodotorula have been isolated from deep-sea tubeworms and
clams by Nagahama et al. (2003a) and have also been recovered from a range of eDNA and culturing studies derived from deep-sea samples (Nagahama et al. 2001, 2003a) (Figure 4). Although
they have not been directly shown to be parasitic agents, they appear to be closely associated with
certain marine invertebrates (Nagahama et al. 2003a). Similarly, black yeast (Herpotrichiellaceae
of the order Chaetothyriales) has been proposed as a causal agent in disease of the deep-sea mussel
Bathymodiolus brevior in the Fiji Basin (Van Dover et al. 2007). Other known fungal pathogens
closely related to terrestrial fungi are particularly prevalent in marine mammals, including Aspergillus (aspergillosis), Blastomyces (blastomycosis), Coccidioides (coccidioidomycosis), Cryptococcus
(cryptococcosis), Candida (candidiasis), Fusarium (fusariomycosis), Histoplasma, Sporothrix, dermatitis caused by Malassezia, and a diverse group of disease-causing zygomycetes (Higgins 2000).
Many of these groups are frequently recovered by eDNA analysis (e.g., Bass et al. 2007, Edgcomb
et al. 2002, Jebaraj et al. 2009), confirming their widespread presence in marine environments
(Figures 1–4).
Fungi generally have been shown to associate with coral and are suggested to represent
opportunistic pathogens of corals weakened by environmental stress (Le Campion-Alsumard
et al. 1995). For example, Aspergillus sydowii (shown in Figure 1) is closely related to terrestrial
Aspergillus species and has been identified as a pathogen of sea fan corals (Alker et al. 2001, Shinn
et al. 2000). Such corals are known to release defensive chemicals during infection by endoliths
such as A. sydowii (Alker et al. 2001).
Cawthorn (2011) identified the ascomycete fungus Fusarium as a disease-causing agent in
American lobsters (Fusarium is also represented in multiple marine eDNA analyses; see Figure 1),
noting its opportunistic nature and propensity to invade through damaged or dead tissues
(Cawthorn 2011). In a review of emerging diseases and their links to climate and anthropogenic
512
Richards et al.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
18:0
factors, Harvell and coauthors (1999) found that three of 34 mass mortalities in marine environments are attributed to fungi.
Wang & Johnson (2009) pointed out that studies of fungal pathogens of marine algae mostly
focus on seaweed or macroalgae and also rely on cultivation-based methods, which can give a
false impression of natural diversity. This means that culture-independent molecular probing of
potentially infected tissue could reveal important new information about organismal interactions of
marine fungi. Several dozen ascomycete fungi are already known to be pathogens of marine algae
(Kohlmeyer & Kohlmeyer 1979), while chytrids (e.g., Chytridium polysiphoniae) are also known
to parasitize macroalgae (Küpper et al. 2006). Seaweeds have been shown to respond to fungal
attack, by the production of antifungal lobophorolide and tolytoxin by the brown alga Lobophora
variegata against the parasitic ascomycetes Lindra thalassiae and Dendryphiella salina (Kubanek et al.
2003). Many ascomycetes appear to be specific to red, green, or brown algae, although some are
generalists. Some cause galls on seaweeds, whereas others are involved in symbioses with seaweeds,
outside of which neither partner appears able to grow. For example, the ascomycete Mycophycias
ascophylli is involved in a three-way symbiosis with the phaeophyte Ascophyllum nodosum and its red
algal epiphyte Polysiphonia lanosa. The fungus interacts with both, possibly transferring nutrients
between them (Spooner & Roberts 2005).
Another relatively well-studied set of interactions is between sponges and fungi. A culturebased study by Li & Wang (2009) revealed a large diversity of fungi associated with sponge species
(e.g., Mycosphearellales, Eurotialies, Dothideales, Hypocreales, Diapothales, Xylariales, Pleosporales, Aphyllophorales, and Saccharomycetales). They were able to classify their isolates into three
categories: those found in all sponge species, those in more than one but not all, and specialists
found only in a single sponge species. Cladosporium, Penicillium, Aspergillus, and Eupenicillium were
recovered from the majority of sponges investigated, suggesting that fungi from these groups are
regularly associated with sponges. Again, these phylogenetic groups are consistently recovered
in marine eDNA analyses, and many of the lineages are closely related to nonmarine species
(Figure 1).
The isolation-independent denaturing gradient gel electrophoresis approach used by Gao et al.
(2008) also showed a high diversity of fungi associated with sponges, and demonstrated that fungal
communities differed between sponge species and between sponges and the surrounding seawater.
They found a high incidence and microdiversity of Malassezia lineages. Malassezia are ubiquitous
lipophilic yeasts and are found in soils, sediments, and deep-sea habitats and on terrestrial metazoa.
Gao et al. (2008) suggested that their analysis of sponges had detected the highest diversity to date
of Malassezia lineages from a single host. It is currently unclear whether the diversity of spongeassociated fungi represents symbionts and/or parasites.
Our phylogenetic analysis also demonstrated a large number of Malassezia-like sequences recovered from a number of marine environments, including deep-sea water column and sediment
samples. These sequences formed a large clade displaying complex microvariation, suggesting a
radiation of marine Malassezia lineages and suggesting that this represents an important and diverse group of fungi in marine environments (Figure 3; also see Bass et al. 2007, Edgcomb et al.
2011, Jebaraj et al. 2009, López-Garcia et al. 2007).
Fungi as Saprotrophic Agents in the Marine Environment
In terrestrial ecosystems, fungi perform critical roles as saprotrophs in detrital environments,
breaking down complex biopolymers and recycling nutrients. This process is important because it
underpins the wider ecosystem, but it is much less clear which organisms perform equivalent roles
in marine environments. Marine yeasts are generally associated with nutrient concentrations [e.g.,
www.annualreviews.org • Marine Fungi
513
ARI
3 November 2011
18:0
pollution, plankton blooms, and macroalgae (Kohlmeyer & Kohlmeyer 1979)], suggesting that
fungi are also important saprotrophs in marine environments. Furthermore, saprotrophy and life in
detritus are often associated with anoxic or partially anoxic conditions, and fungi have been shown
to possess a range of cellular and genomic adaptations to anoxic environments (discussed briefly
above). Therefore, although marine fungal diversity appears to be limited compared to terrestrial
environments (Kis-Papo 2005, Massana & Pedrós-Alió 2008, Richards & Bass 2005), fungi may
still play a critical role in detritus processing in marine ecosystems (Mann 1988, Raghukumar
2004), thus providing essential nutrients to the wider food web, such as the amino acids lysine
and methionine, various vitamins, polyunsaturated fatty acids, and sterols (an important precursor
for the manufacture of cholesterols in marine animals) (Phillips 1984). These pathways, through
which organic matter re-enters the food web, are vital for the survival of detritivorous animals,
which are unable to synthesize such compounds by themselves (Raghukumar 2004). For example,
Crustacea require the polyunsaturated fatty acid docosahexaenoic acid for growth (Harrison 1990),
which is provided to benthic food webs by detrital microbes (Raghukumar 2004), although it is
not clear whether true fungi mediate this process. In addition, fungi are thought to play a role in
the degradation of tucinin, an animal cellulose, which occurs in the test of tunicates (Kohlmeyer &
Kohlmeyer 1979). Indeed, phylogenetic analysis of environmental marine fungal sequences shows
a number of sequences branching closely to known saprotrophic fungi, including, for example,
Aspergillus (Figure 1), Fusarium (Figure 1), Coprinus (Figure 3), and Exidia (Figure 3).
One relatively strong research focus regarding marine fungal interactions has been the breakdown of calcareous structures by fungi, whether of living or dead organisms. Marine fungi are
known to degrade structures such as mollusc shells, burrow linings, and barnacle shells (Hyde
et al. 1998). For example, the ascomycete genera Arenariomyces, Corollospora, and Lindra degrade
foraminiferan tests and, with related genera including Remispora, attack other calcareous structures, for example, those of barnacles and shipworms (Spooner & Roberts 2005). Other endolithic
fungi (the general term for those living inside rocks and boring into calcareous substances) associated with many coral genera include basidiomycetes, many ascomycetes (e.g., A. sydowii ), and the
chytrids Dodgella priscus and Conchyliastrum enderi. Ostracoblabe and Lithopythium are often cited as
endolithic fungi (Golubic et al. 2005, Kendrick et al. 1982), although sequence data for all four of
these genera are currently unavailable in GenBank.
Fungi may also be important in degrading lignocellulose in marine environments, as they are
in terrestrial ones. They are able to tolerate reduced oxygen concentrations (discussed above)
and could potentially be the main degrader of these compounds in low-oxygen and anoxic marine sediments (Hyde et al. 1998) and of plant material in the oceans in general, especially in
mangrove ecosystems. Evidence for lignocellulose degradation by marine fungi (through the production of endoglucanase enzymes, allowing growth on a carboxymethylcellulose substrate) has
been found in over 30 strains of phylogenetically diverse fungi isolated from marine environments
(Hyde et al. 1998). Mangrove leaves are rich in lignocellulosic structural polymers, soluble organics, phenolics, and tannins, making them highly resistant to degradation from many microbes.
However, fungi such as Pestalotiopsis and Cladosporium—common primary saprotrophs—are often recovered from mangrove leaves (Raghukumar 2004). The initial production of degrading
enzymes by fungal colonizers therefore likely plays a vital role in the breakdown of robust plant
materials.
Fungal strains isolated from leaves of Spartina alterniflora have proven capable of cellulose,
cellobiose, pectin, lipid, tannic acid, starch, and xylan degradation (Gessner 1980). Suetrong et al.
(2009) reported a diversity of intertidal marine Dothideomycetes mainly associated with mangrove
habitats in tropical/subtropical environments, noting that these species are well adapted to marine
environments with active discharge of ascospores and with a mucilaginous sheath. A representative
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
514
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
18:0
diversity of species associated with mangrove plants is summarized in Figure 1, showing the wide
diversity of Dothideomycetes fungi associated with this marine environment (Suetrong et al.
2009). Dothideomycetes are frequently found as saprobes on decaying woody material in marine
environments. They are also parasites or symbionts of seagrasses or marine algae. Suetrong et al.
(2009) therefore posed the question of whether this pattern represents a radiation, or multiple
radiations, of Dothideomycetes specifically in mangrove marine habitats.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Filling the Fungal Niche in the Marine Ecosystems: Fungal Analogs
The relative contribution of fungi to disease load and saprotrophic operations within marine
ecosystems has been obscured by the high incidence of and taxonomic confusion caused by organisms that have fungal-like characteristics but are not true fungi (Cavalier-Smith 1987, CavalierSmith & Chao 2006), i.e., those that do not branch within the fungal clade within the opisthokont
supergroup (Adl et al. 2005, Simpson & Roger 2004). These fungi-like organisms also feed by
osmotrophy, in many cases forming polarized cells analogous to hyphae and rhizoids of true fungi,
and grow on standard fungal growth media; hence they are often recovered during culture-based
analyses of environmental diversity and have historically been considered to be fungi. However,
these fungal-like organisms have evolved this lifestyle independently and possess cellular characteristics that separate them from true fungi. For example, true fungi generally form a robust
exoskeleton containing chitin during part of their life cycle however, the exoskeleton of the nonfungal analogs does not contain chitin (Bartnicki-Garcia 1987).
Fungal analogs include oomycetes; Pirsonia; hyphochytriomycetes [collectively forming the
pseudofungi (Cavalier-Smith & Chao 2006)]; labyrinthulids and thraustochytrids (which are stramenopiles); ichthyosporeans (e.g., Ichthyophonus), which also branch within the opisthokonts but
separately from true fungi; and endomyxan Cercozoa [ascetosporeans (e.g., Paradinium and Haplosporidium) and phytomyxids (plasmodiophorids and phagomyxids)]. All these groups have at some
stage been classified as true fungi. Ascetosporea are well known for causing MSX disease of oysters
and other diseases of marine invertebrates; plasmodiophorids and their sister group phagomyxids
are important marine parasites of seagrasses, diatoms, and phaeophycean algae (e.g., Parodi et al.
2010).
Indeed, general surveys of marine fungi, both recent and from earlier in the twentieth century,
report more fungal analogs than true fungi, thereby implying that true fungi are relatively unimportant in marine habitats. For example, a comprehensive review of marine fungi from Woods Hole by
Sparrow (1936) described mostly oomycetes, along with labyrinthulids, a thraustochytrid, Protomyxa (an unclassified large branched amoeba, probably endomyxan), and the chytrid Chytridium—
the only true fungus listed (Figure 5; also see Sparrow 1936). A similarly comprehensive review
of zoosporic fungal parasites of marine biota (Raghukumar 1996) described many pseudofungal
groups, including 11 genera of oomycetes infecting diatoms, green, red, and brown algae, and
crustaceans, and also hyphochytriomycetes, including members of the genus Anisolpidium, parasitizing filamentous brown algae, and Hyphochytridium peniliae, causing mycosis of the planktonic
cladoceran Penilia avirostris.
Labyrinthulids and thraustochytrids (e.g., Schizochytrium, Ullkenia, Labyrinthula, Labyrinthuloides) are generally considered exclusively marine, although more recently labyrinthulids have been
found in nonmarine habitats (Douhan et al. 2009). These stramenopiles parasitize a wide range
of marine organisms, including diatoms, octopus, squid, seagrasses, shellfish, and fish. Thraustochytrids have been detected on marine substrates such as salp fecal pellets and marine snow.
They reproduce through the production of motile zoospores, which swim to a food source and
colonize it (in an analogous manner to fungal chytrids). There is also evidence of saprotrophic
www.annualreviews.org • Marine Fungi
Pseudofungi: group
of stramenopiles
(heterokonts)
unrelated to true fungi
but that feed and grow
using analogous
methods to true fungi
Labyrinthulids and
thraustochytrids:
stramenopile
(heterokont) protists
with partially similar
morphologies and
analogous life cycles to
chytrid fungi; produce
a network of filaments
for feeding and
movement
Endomyxa: a
diverse group of filose
amoebae, parasites,
and uncharacterized
environmental
sequences currently
included within the
phylum Cercozoa
(supergroup Rhizaria),
comprising the sister
group to core
Cercozoa
Marine snow:
organic detritus falling
from the upper water
column layers, often
comprising mucus
secreted by
phytoplankton, most
prolifically diatoms
(which form
aggregations in the
water column)
Erratum
515
MA04CH20-Richards
ARI
3 November 2011
18:0
function among fungal analogs, and studies within mangrove swamps reveal the colonization of
fallen leaves by the oomycete Halophytophthora sp. of red mangrove plants within two hours of
submergence (Raghukumar 2004).
SUMMARY POINTS
1. Currently known fungal diversity in marine environments represents a tiny fraction of
that from terrestrial environments.
2. Fungal sequences detected in marine environments span a large diversity of forms and
lineages, including chytrids, filamentous hyphal forms, and multicellular forms.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
3. Dikarya yeast forms appear to dominate the known diversity of marine fungi.
4. Marine environments, like freshwater environments, harbor a number of highly divergent, deep-branching, and uncultured fungi, of which future study will greatly improve
our understanding of fungal cell diversity and evolution.
5. There appears to have been frequent marine-terrestrial and terrestrial-marine colonization events during the radiation of the Fungi.
6. Fungi play diverse ecological roles in marine ecosystems and have frequently been associated with parasitism of marine animals, plants, and algae.
7. Many ecological niches inhabited by true fungi in terrestrial and freshwater habitats are
occupied by diverse fungal analogs in marine habitats.
8. Fungal-specific molecular studies in marine environments are so far relatively few, yet
many reveal a marine fungal diversity that is significantly higher than other methods
suggest but much less diverse than terrestrial environments.
FUTURE ISSUES
1. What are the main drivers of detrital and saprotrophic processes in marine environments?
2. What is the diversity of true fungal parasites in marine environments, and what dangers
do they represent for marine conservation?
3. What is the true diversity of lower fungi in marine environments, and how do they relate
to terrestrial taxa and the fungal tree of life?
4. What are the evolutionary and physiological changes between truly marine fungi and
their close terrestrial relatives?
5. Do fungal analogs perform the majority of saprotrophic functions in marine environments?
6. Do fungal analogs actually exclude true fungi from colonizing apparently suitable marine
habitats?
7. By what evolutionary mechanisms have fungal analogs been able to occupy fungal-like
niches in marine habitats?
516
Richards et al.
MA04CH20-Richards
ARI
3 November 2011
18:0
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
This work was primarily supported by the European Funding Agencies from the ERA-net program
BiodivERsA, under the BioMarKs project. The authors are supported by research grants from the
Biotechnology and Biological Sciences Research Council (BBSRC), Department for Environment,
Food and Rural Affairs (DEFRA), and Natural Environment Research Council (NERC).
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
LITERATURE CITED
Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, et al. 2005. The new higher level classification
of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399–451
Alker AP, Smith GW, Kim K. 2001. Characterization of Aspergillus sydowii (Thom et Church), a fungal
pathogen of Caribbean sea fan corals. Hydrobiologia 460:105–11
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol.
215:403–10
Anderson IC, Campbell CD, Prosser JI. 2003. Potential bias of fungal 18S rDNA and internal transcribed
spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. Environ. Microbiol.
5:36–47
Bartnicki-Garcia S. 1987. The cell wall: a crucial structure in fungal evolution. In Evolutionary Biology of the
Fungi, ed. ADM Rayner, CM Brasier, D Moore, pp. 389–403. Cambridge, UK: Cambridge Univ. Press
Bass D, Cavalier-Smith T. 2004. Phylum-specific environmental DNA analysis reveals remarkably high global
biodiversity of Cercozoa (Protozoa). Int. J. Syst. Evol. Microbiol. 54:2393–404
Bass D, Howe A, Brown N, Barton H, Demidova M, et al. 2007. Yeast forms dominate fungal diversity
in the deep oceans. Proc. Biol. Sci. 274:3069–77
Berbee ML, Taylor JW. 2010. Dating the molecular clock in fungi: How close are we? Fungal Biol. Rev.
24:1–16
Berney C, Fahrni J, Pawlowski J. 2004. How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of
environmental DNA surveys. BMC Biol. 2:13
Bruns TD, Gardes M. 1993. Molecular tools for the identification of ectomycorrhizal fungi–taxon-specific
oligonucleotide probes for suilloid fungi. Mol. Ecol. 2:233–42
Buchan A, Newell SY, Moreta JI, Moran MA. 2002. Analysis of internal transcribed spacer (ITS) regions of
rRNA genes in fungal communities in a southeastern U.S. salt marsh. Microb. Ecol. 43:329–40
Buée M, Reich M, Murat C, Morin E, Nilsson RH, et al. 2009. 454 pyrosequencing analyses of forest soils
reveal an unexpectedly high fungal diversity. New Phytol. 184:449–56
Burgaud G, Le Calvez T, Arzur D, Vandenkoornhuyse P, Barbier G. 2009. Diversity of culturable
marine filamentous fungi from deep-sea hydrothermal vents. Environ. Microbiol. 11:1588–600
Cavalier-Smith T. 1987. The origin of fungi and pseudofungi. In Evolutionary Biology of the Fungi, ed. ADM
Rayer, pp. 339–53. Br. Mycol. Soc. Symp. Cambridge, UK: Cambridge Univ. Press
Cavalier-Smith T. 2004. Only six kingdoms of life. Proc. Biol. Sci. 271:1251–62
Cavalier-Smith T, Chao EE. 2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom
Chromista). J. Mol. Evol. 62:388–420
Cawthorn RJ. 2011. Diseases of American lobsters (Homarus americanus): a review. J. Invertebr. Pathol. 106:71–
78
Chambouvet A, Morin P, Marie D, Guillou L. 2008. Control of toxic marine dinoflagellate blooms by serial
parasitic killers. Science 322:1254–57
Curtis TP, Sloan WT, Scannell JW. 2002. Estimating prokaryotic diversity and its limits. Proc. Natl. Acad.
Sci. USA 99:10494–99
www.annualreviews.org • Marine Fungi
Presents the first
fungal-specific clone
library approach to
investigating fungal
diversity in deep-sea
environments,
suggesting that yeasts
and parasites dominate.
Presents a large-scale
culturing experiment of
fungal isolates from
deep-sea hydrothermal
vents, demonstrating
the presence of a wide
diversity of Dikarya.
517
MA04CH20-Richards
ARI
3 November 2011
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Using DNA and RNA,
demonstrates that a low
diversity of Dikarya
yeasts dominate
eukaryotic community
in deep-sea sediments.
Represents a leading
attempt to evaluate the
extent of the fungal
kingdom.
518
18:0
Dawson SC, Pace NR. 2002. Novel kingdom-level eukaryotic diversity in anoxic environments. Proc. Natl.
Acad. Sci. USA 99:8324–29
Douhan GW, Olsen MW, Herrel MW, Winder C, Wong F, Entwistle K. 2009. Genetic diversity of
Labyrinthula terrestris, a newly emergent plant pathogen, and the discovery of new Labyrinthula organisms.
Mycol. Res. 113:1192–99
Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity.
BMC Bioinform. 5:113
Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A. 2011. Marine subsurface eukaryotes: the
fungal majority. Environ. Microbiol. 13:172–83
Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML. 2002. Benthic eukaryotic diversity in the
Guaymas Basin hydrothermal vent environment. Proc. Natl. Acad. Sci. USA 99:7658–62
Embley TM. 2006. Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philos. Trans. R. Soc.
Lond. B Biol. Sci. 361:1055–67
Galtier N, Gouy M, Gautier C. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543–48
Gao Z, Li B, Zheng C, Wang G. 2008. Molecular detection of fungal communities in the Hawaiian marine
sponges Suberites zeteki and Mycale armata. Appl. Environ. Microbiol. 74:6091–101
Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the
identification of mycorrhizae and rusts. Mol. Ecol. 2:113–18
Gargas A, DePriest PT, Grube M, Tehler A. 1995. Multiple origins of lichen symbioses in fungi suggested
by SSU rDNA phylogeny. Science 268:1492–95
Gessner RV. 1980. Degradative enzyme production by salt-marsh fungi. Bot. Mar. 23:133–39
Giovannoni SJ, Britschgi TB, Moyer CL, Field KG. 1990. Genetic diversity in Sargasso Sea bacterioplankton.
Nature 345:60–63
Gojkovic Z, Knecht W, Zameitat E, Warneboldt J, Coutelis JB, et al. 2004. Horizontal gene transfer
promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol. Genet.
Genomics 271:387–93
Golubic S, Radtke G, Le Campion-Alsumard T. 2005. Endolithic fungi in marine ecosystems. Trends Microbiol.
13:229–35
Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum
likelihood. Syst. Biol. 52:696–704
Hall C, Brachat S, Dietrich FS. 2005. Contribution of horizontal gene transfer to the evolution of Saccharomyces
cerevisiae. Eukaryot. Cell 4:1102–15
Harrison KE. 1990. The role of nutrition in maturation, reproduction and embryonic development of decapod
crustaceans: a review. J. Shellfish Res. 9:1–28
Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, et al. 1999. Emerging marine diseases: climate
links and anthropogenic factors. Science 285:1505–10
Hawksworth DL. 1991. The fungal dimension of biodiversity: magnitude, significance and conservation. Mycol. Res. 95:641–55
Hawksworth DL. 2001. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol.
Res. 105:1422–32
Held AA. 1981. Rozella and Rozellopsis: naked endoparasitic fungi which dress up as their hosts. Bot. Rev.
47:451–515
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, et al. 2007. A higher-level phylogenetic
classification of the Fungi. Mycol. Res. 111:509–47
Higgins R. 2000. Bacteria and fungi of marine mammals: a review. Can. Vet. J. 41:105–16
Hirt RP, Healy B, Vossbrinck CR, Canning EU, Embley TM. 1997. A mitochondrial HSP70 orthologue
in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol.
7:995–98
Hirt RP, Logsdon JM Jr, Healy B, Dorey MW, Doolittle WF, Embley TM. 1999. Microsporidia are related
to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl. Acad.
Sci. USA 96:580–85
Richards et al.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
18:0
Horton TR, Bruns TD. 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the blackbox. Mol. Ecol. 10:1855–71
Hyde KD, Jones EBG, Leaño E, Pointing SB, Poonyth AD, et al. 1998. Role of fungi in marine ecosystems.
Biodivers. Conserv. 7:1147–61
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. 2006a. Reconstructing the early evolution
of Fungi using a six-gene phylogeny. Nature 443:818–22
James TY, Letcher PM, Longcore JE, Mozley-Standridge SE, Porter D, et al. 2006b. A molecular
phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98:860–71
Jebaraj CS, Raghukumar C. 2009. Anaerobic dentrification in fungi from the coastal marine sediments off
Goa, India. Mycol. Res. 113:100–9
Jebaraj CS, Raghukumar C, Behnke A, Stoeck T. 2009. Fungal diversity in oxygen-depleted regions of the
Arabian Sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microbiol.
Ecol. 71:399–412
Jones MDM, Forn I, Gadelha C, Egan MJ, Bass D, et al. 2011. Discovery of novel intermediate forms redefines
the fungal tree of life. Nature 474:200–3
Jumpponen A, Jones KL. 2009. Massively parallel 454 sequencing indicates hyperdiverse fungal communities
in temperate Quercus macrocarpa phyllosphere. New Phytol. 184:438–48
Keeling PJ. 2003. Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete
origin of microsporidia. Fungal Genet. Biol. 38:298–309
Kendrick B, Rick MJ, Michaelides J, Bergman K. 1982. Amphibious microborers: bioeroding fungi isolated
from live corals. Bull. Marine Sci. 32:862–67
Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008. Dictionary of the Fungi. Wallingford, UK: CABI
Kis-Papo T. 2005. Marine fungal communities. In The Fungal Community: Its Organisation and Role in the
Ecosystem, ed. J Dighton, JF White, P Oudemans, pp. 61–92. Boca Raton, FL: Taylor & Francis
Kohlmeyer J, Kohlmeyer E. 1979. Marine Mycology: The Higher Fungi. New York: Academic
Kubanek J, Jensen PR, Keifer PA, Sullards MC, Collins DO, Fenical W. 2003. Seaweed resistance to microbial
attack: a targeted chemical defence against marine fungi. Proc. Natl. Acad. Sci. USA 100:6916–21
Küpper FC, Maier I, Müller DG, Loiseaux-de Goer S, Guillou L. 2006. Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae
Cohn. Cryptogam. Algol. 27:165–84
Lara E, Moreira D, López-Garcia P. 2010. The environmental clade LKM11 and Rozella form the deepest
branching clade of Fungi. Protist 161:116–21
Le Calvez T, Burgaud G, Mahé S, Barbier G, Vandenkoornhuyse P. 2009. Fungal diversity in deep-sea
hydrothermal ecosystems. Appl. Environ. Microbiol. 75:6415–21
Le Campion-Alsumard T, Golubic S, Priess K. 1995. Fungi in corals: symbiosis or disease? Interaction between
polyps and fungi causes perl-like skeleton biomineralization. Mar. Ecol. Prog. Ser. 117:137–47
Lef èvre E, Bardot C, Noël C, Carrias JF, Viscogliosi E, et al. 2007. Unveiling fungal zooflagellates as members
of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ.
Microbiol. 9:61–71
Lef èvre E, Roussel B, Amblard C, Sime-Ngando T. 2008. The molecular diversity of freshwater
picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS ONE 3:e2324
Lefranc M, Thénot A, Lepère C, Debroas D. 2005. Genetic diversity of small eukaryotes in lakes differing by
their trophic status. Appl. Environ. Microbiol. 71:5935–42
Lepère C, Boucher D, Jardillier L, Domaizon I, Debroas D. 2006. Succession and regulation factors of
small eukaryote community composition in a lacustrine ecosystem (Lake Pavin). Appl. Environ. Microbiol.
72:2971–81
Li Q, Wang G. 2009. Diversity of fungal isolates from three Hawaiian marine sponges. Mycol. Res. 164:233–41
Liu Y, Steenkamp ET, Brinkmann H, Forget L, Philippe H, Lang BF. 2009. Phylogenomic analyses predict
sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support.
BMC Evol. Biol. 9:272
Lockhart PJ, Steel MA, Hendy MD, Penny D. 1994. Recovering evolutionary trees under a more realistic
model of sequence evolution. Mol. Biol. Evol. 11:605–12
www.annualreviews.org • Marine Fungi
Presents progress in
understanding the
complexity of chytrid
fungi, vital for
understanding the
diversity of lower fungi
SSU sequences
recovered from eDNA.
Proposes that fungi play
a significant role in the
microbial loop in
freshwater ecosystems.
519
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
Presents work
demonstrating a wide
diversity of yeasts in
deep-sea environments
often associated with
animals.
Demonstrates that
sequencing rDNA
markers from soil
environments radically
extends diversity
estimates for the Fungi.
520
18:0
López-Garcı́a P, Rodriguez-Valera F, Pedrós-Alió C, Moreira D. 2001. Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–7
López-Garcı́a P, Vereshchaka A, Moreira D. 2007. Eukaryotic diversity associated with carbonates and fluidseawater interface in Lost City hydrothermal field. Environ. Microbiol. 9:546–54
Mann KH. 1988. Production and use of detritus in various freshwater, estuarine, and coastal marine ecosystems.
Limnol. Oceanogr. 33:910–30
Massana R, Balagué M, Guillou L, Pedrós-Alió C. 2004a. Picoeukaryotic diversity in an oligotrophic coastal
site studied by molecular and culturing approaches. FEMS Microbiol. Ecol. 50:231–43
Massana R, Castresana J, Balagué V, Guillou L, Romari K, et al. 2004b. Phylogenetic and ecological analysis
of novel marine stramenopiles. Appl. Environ. Microbiol. 70:3528–34
Massana R, Pedrós-Alió C. 2008. Unveiling new microbial eukaryotes in the surface ocean. Curr. Opin.
Microbiol. 11:213–18
May RM. 1991. Fondness for Fungi. Nature 352:475–76
May RM. 1994. Conceptual aspects of quantification of the extent of biological diversity. Philos. Trans. R. Soc.
Lond. B Biol. Sci. 345:13–20
Moon-van der Staay SY, De Wachter R, Vaulot D. 2001. Oceanic 18S rDNA sequences from picoplankton
reveal unsuspected eukaryotic diversity. Nature 409:607–10
Moreira D, López-Garcı́a P. 2002. The molecular ecology of microbial eukaryotes unveils a hidden world.
Trends Microbiol. 10:31–38
Mueller GM, Schmit JP. 2007. Fungal biodiversity: What do we know? What can we predict? Biodivers.
Conserv. 16:1–5
Mueller GM, Schmit JP, Leacock PR, Buyck B, Cifuentes J, et al. 2007. Global diversity and distribution of
macrofungi. Biodivers. Conserv. 16:37–48
Nagahama T, Hamamoto M, Nakase T, Horikoshi K. 2003a. Rhodotorula benthica sp. nov. and
Rhodotorula calyptogenae sp. nov., novel yeast species from animals collected from the deepsea floor, and Rhodotorula lysiniphila sp. nov., which is related phylogenetically. Int. J. Syst. Evol.
Microbiol. 53:897–903
Nagahama T, Hamamoto M, Nakase T, Takaki Y, Horikoshi K. 2003b. Cryptococcus surugaensis sp. nov., a
novel yeast species from sediment collected on the deep-sea floor of Suruga Bay. Int. J. Syst. Evol. Microbiol.
53:2095–98
Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K. 2001. Distribution and identification of red
yeasts in deep-sea environments around the northwest Pacific Ocean. Antonie van Leeuwenhoek 80:101–10
Newell SY. 1996. Established and potential impacts of eukaryotic mycelial decomposers in marine/terrestrial
ecotones. J. Exp. Mar. Biol. Ecol. 200:187–206
Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH. 2008. Intraspecific ITS variability in the
kingdom fungi as expressed in the international sequence databases and its implications for molecular
species identification. Evol. Bioinform. 4:193–201
Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson KH, Kõljalg U. 2006. Taxonomic reliability
of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1:e59
O’Brien HE, Parrent JL, Jackson JA, Moncalvo J-M, Vilgalys R. 2005. Fungal community analysis by
large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 71:5544–50
Olsen GJ, Lane DJ, Giovannoni SJ, Pace NR, Stahl DA. 1986. Microbial ecology and evolution: a ribosomal
RNA approach. Annu. Rev. Microbiol. 40:337–65
Pace NR. 1997. A molecular view of microbial diversity and the biosphere. Science 276:734–40
Parodi ER, Caceres EJ, Westermeirer R, Müller DG. 2010. Secondary zoospores in the algal endoparasite
Maullinia ectocarpii (Plasmodiophoromycota). Biocell 34:45–52
Pawlowski J, Christen R, Lecroq B, Bachar D, Shahbazkia HR, et al. 2011. Eukaryotic richness in the abyss:
insights from pyrotag sequencing. PLoS ONE 6:e18169
Phillips NW. 1984. Role of different microbes and substrates as potential suppliers of specific, essential
nutrients to marine detritivores. Bull. Mar. Sci. 35:283–98
Pirozynski KA, Malloch DW. 1975. The origin of land plants: a matter of mycotrophism. Biosystems 5:153–64
Richards et al.
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
MA04CH20-Richards
ARI
3 November 2011
18:0
Porter TM, Schadt CW, Rizvi L, Martin AP, Schmidt SK, et al. 2008. Widespread occurrence and phylogenetic
placement of a soil clone group adds a prominent new branch to the fungal tree of life. Mol. Phylogenet.
Evol. 46:635–44
Raghukumar C. 1988. Zoosporic fungal parasites of marine biota. In Advances in Zoosporic Fungi ed.R Dayal,
pp. 61–80. New Delhi: MD Publ.
Raghukumar S. 2004. The role of fungi in marine detrital processes. In Marine Microbiology: Facets and Opportunities, ed. N Ramaiah, pp. 91–101. Goa, India: Natl. Inst. Oceanogr.
Rappé MS, Giovannoni SJ. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369–94
Richards TA, Bass D. 2005. Molecular screening of free-living microbial eukaryotes: diversity and distribution
using a meta-analysis. Curr. Opin. Microbiol. 8:240–52
Richards TA, Vepritskiy AA, Gouliamova D, Nierzwicki-Bauer SA. 2005. The molecular diversity of freshwater picoeukaryotes from an oligotrophic lake reveals diverse, distinctive and globally dispersed lineages.
Environ. Microbiol. 7:1413–25
Schadt CW, Martin AP, Lipson DA, Schmidt SK. 2003. Seasonal dynamics of previously unknown fungal
lineages in tundra soils. Science 301:1359–61
Selosse MA, Le Tacon F. 1998. The land flora: a phototroph-fungus partnership? Trends Ecol. Evol. 13:15–20
Shinn EA, Smith GA, Prospero JM, Betzer P, Hayes ML, et al. 2000. African dust and the demise of Carribean
coral reefs. Geophys. Res. Lett. 27:3029–32
Shoun H, Kim DH, Uchiyama H, Sugiyama J. 1992. Dentrification by fungi. FEMS Microbiol. Lett.
94:277–81
Simon L, Bousquet J, Levesque RC, Lalonde M. 1993. Origin and diversification of endomycorrhizal fungi
and coincidence with vascular land plants. Nature 363:67–69
Simonato F, Campanaro S, Lauro FM, Vezzi A, D’Angelo M, et al. 2006. Pezophilic adaptation: a genomic
point of view. J. Biotechnol. 126:11–25
Simpson AG, Roger AJ. 2004. The real ‘kingdoms’ of eukaryotes. Curr. Biol. 14:R693–96
Slapeta J, Moreira D, López-Garcı́a P. 2005. The extent of protist diversity: insights from molecular ecology
of freshwater eukaryotes. Proc. R. Soc. Lond. B Biol. Sci. 272:2073–81
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, et al. 2006. Microbial diversity in the deep sea
and the underexplored “rare biosphere.” Proc. Natl. Acad. Sci. USA 103:12115–20
Sparrow FKJ. 1936. Biological observations on marine fungi of Woods Hole waters. Biol. Bull. 70:236–63
Spatafora J, Volkmann-Kohlmeyer B, Kohlmeyer E. 1998. Independent terrestrial origins of the
Halosphaeriales (marine Ascomycota). Am. J. Bot. 85:1569–80
Spooner B, Roberts P. 2005. Fungi. London: Collins
Stoeck T, Bass D, Nebel M, Christen R, Jones MD, et al. 2010. Multiple marker parallel tag environmental
DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol.
19:21–31
Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS. 2006. A multiple PCR-primer approach to access
the microeukaryotic diversity in environmental samples. Protist 157:31–43
Suetrong S, Schoch CL, Spatafora JW, Kohlmeyer J, Volkmann-Kohlmeyer B, et al. 2009. Molecular systematics of the marine Dothideomycetes. Stud. Mycol. 64:155–73
Takaya N, Suzuki S, Kuwazaki S, Shoun H, Maruo F, et al. 1999. Cytochrome p450nor, a novel class of
mitochondrial cytochrome P450 involved in nitrate respiration in the fungus Fusarium oxysporum. Arch.
Biochem. Biophys. 372:340–46
Takishita K, Miyake H, Kawato M, Maruyama T. 2005. Genetic diversity of microbial eukaryotes in anoxic
sediment around fumaroles on a submarine caldera floor based on the small-subunit rDNA phylogeny.
Extremophiles 9:185–96
Takishita K, Tsuchiya M, Reimer JD, Maruyama T. 2006. Molecular evidence demonstrating the basidiomycetous fungus Cryptococcus curvatus is the dominant microbial eukaryote in sediment at the Kuroshima Knoll
methane seep. Extremophiles 10:165–69
Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T. 2007. Diversity of microbial eukaryotes in
sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples
and two enrichment cultures. Extremophiles 11:563–76
www.annualreviews.org • Marine Fungi
Erratum
Presents phylogenetic
evidence for
terrestrial-to-marine
transitions in the
ascomycetes.
521
MA04CH20-Richards
ARI
3 November 2011
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Presents evidence that
fungi cause disease in
deep-sea bivalves.
522
18:0
Uchimura H, Enjoji H, Seki T, Taguchi A, Takaya N, Shoun H. 2002. Nitrate reductase-formate dehydrogenase couple involved in the fungal denitrification by Fusarium oxysporum. J. Biochem. 131:579–86
Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW. 2002. Extensive fungal diversity in plant
roots. Science 295:2051
Van Dover CL, Ward ME, Scott JL, Underdown J, Andersen B, et al. 2007. A fungal epizootic in
mussels at a deep-sea hydrothermal vent. Mar. Ecol. 28:54–62
van Hannen EJ, Mooij W, van Agterveld MP, Gons HJ, Laanbroek HJ. 1999. Detritus-dependent development
of the microbial community in an experimental system: qualitative analysis by denaturing gradient gel
electrophoresis. Appl. Environ. Microbiol. 65:2478–84
Vilgalys R. 2003. Taxonomic misidentification in public DNA databases. New Phytol. 160:4–5
Wang B, Qiu YL. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza
16:299–363
Wang G, Johnson ZI. 2009. Impact of parasitic fungi on the diversity and functional ecology of marine
phytoplankton. In Marine Phytoplankton, ed. TW Kersey, SP Munger, pp. 211–28. Hauppauge, NY:
Nova Sci.
Webster J, Weber WS. 2007. Introduction to Fungi. Cambridge, UK: Cambridge Univ. Press
Wuyts J, De Rijk P, Van de Peer Y, Pison G, Rousseeuw P, De Wachter R. 2000. Comparative analysis of
more than 3000 sequences reveals the existence of two pseudoknots in area V4 of eukaryotic small subunit
ribosomal RNA. Nucleic Acids Res. 28:4698–708
Richards et al.
MA04-FrontMatter
ARI
16 November 2011
9:36
Annual Review of
Marine Science
Contents
Volume 4, 2012
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
A Conversation with Karl K. Turekian
Karl K. Turekian and J. Kirk Cochran p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Climate Change Impacts on Marine Ecosystems
Scott C. Doney, Mary Ruckelshaus, J. Emmett Duffy, James P. Barry, Francis Chan,
Chad A. English, Heather M. Galindo, Jacqueline M. Grebmeier, Anne B. Hollowed,
Nancy Knowlton, Jeffrey Polovina, Nancy N. Rabalais, William J. Sydeman,
and Lynne D. Talley p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p11
The Physiology of Global Change: Linking Patterns to Mechanisms
George N. Somero p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p39
Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic Seas
Jacqueline M. Grebmeier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p63
Understanding Continental Margin Biodiversity: A New Imperative
Lisa A. Levin and Myriam Sibuet p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p79
Nutrient Ratios as a Tracer and Driver of Ocean Biogeochemistry
Curtis Deutsch and Thomas Weber p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 113
Progress in Understanding Harmful Algal Blooms: Paradigm Shifts
and New Technologies for Research, Monitoring, and Management
Donald M. Anderson, Allan D. Cembella, and Gustaaf M. Hallegraeff p p p p p p p p p p p p p p p p 143
Thin Phytoplankton Layers: Characteristics, Mechanisms,
and Consequences
William M. Durham and Roman Stocker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177
Jellyfish and Ctenophore Blooms Coincide with Human Proliferations
and Environmental Perturbations
Jennifer E. Purcell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Benthic Foraminiferal Biogeography: Controls on Global Distribution
Patterns in Deep-Water Settings
Andrew J. Gooday and Frans J. Jorissen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 237
vi
MA04-FrontMatter
ARI
16 November 2011
9:36
Plankton and Particle Size and Packaging: From Determining Optical
Properties to Driving the Biological Pump
L. Stemmann and E. Boss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263
Overturning in the North Atlantic
M. Susan Lozier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291
The Wind- and Wave-Driven Inner-Shelf Circulation
Steven J. Lentz and Melanie R. Fewings p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Annu. Rev. Marine. Sci. 2012.4:495-522. Downloaded from www.annualreviews.org
by University of Bristol on 09/13/12. For personal use only.
Serpentinite Mud Volcanism: Observations, Processes,
and Implications
Patricia Fryer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 345
Marine Microgels
Pedro Verdugo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375
The Fate of Terrestrial Organic Carbon in the Marine Environment
Neal E. Blair and Robert C. Aller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 401
Marine Viruses: Truth or Dare
Mya Breitbart p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 425
The Rare Bacterial Biosphere
Carlos Pedrós-Alió p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 449
Marine Protistan Diversity
David A. Caron, Peter D. Countway, Adriane C. Jones, Diane Y. Kim,
and Astrid Schnetzer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 467
Marine Fungi: Their Ecology and Molecular Diversity
Thomas A. Richards, Meredith D.M. Jones, Guy Leonard, and David Bass p p p p p p p p p p p p 495
Genomic Insights into Bacterial DMSP Transformations
Mary Ann Moran, Chris R. Reisch, Ronald P. Kiene, and William B. Whitman p p p p p p 523
Errata
An online log of corrections to Annual Review of Marine Science articles may be found at
http://marine.annualreviews.org/errata.shtml
Contents
vii