Microbial Ecology of Mid-Ocean Ridges
and Back-Arc Basins
Ken Takai1, Satoshi Nakagawa1,2, Anna-Louise Reysenbach2, and Joost Hoek 2
Over the past two decades, microbiologists have gained significant insights into the
diversity and physiology of microbial communities associated with deep-sea hydrothermal systems. Much of the initial research focused on mid-ocean ridge (MOR) systems;
however, because of the greater heterogeneity of vent fluid chemistry and sulfide
structures from back-arc basin (BAB) systems, recent studies have begun to explore the
linkages between geochemistry and microbial diversity in these systems. The impact of
microbes on local fluid chemistry and mineralogy has been recognized, and local fluid
physical-geochemical states and mineralogical properties have significant impacts on
the formation and composition of local microbial communities. Data are being accumulated that enable microbiologists not only to link phylogenetic and physiological
diversity of microbial communities to geological and geochemical settings within a
hydrothermal field, but also to review microbial ecosystems in global deep-sea hydrothermal systems with comparison of representative MOR and BAB systems. In this
review, we briefly outline methods in microbial ecology and microbial ecophysiology
at vents and discuss the patterns of diversity (phylogenetic and physiological) emerging
from studies in the global hydrothermal systems. As this volume is dedicated to BABs,
we highlight several case studies on hydrothermal vent microbial communities in BAB
systems that are comparable to the communities in MOR systems.
1. Introduction
from 4°C to above 80°C) thrive by chemolithoautotrophy
or heterotrophy, utilizing the abundant available inorganic
and organic chemical energy and carbon sources. These
organisms exist as free-living forms within the hydrothermal plumes, within mixed diffuse fluids, and as microbial
mats on sediments; as attached biofilms on invertebrates
and on sulfide mineral particles; and as obligate symbionts
within invertebrate hosts. The effect of microbes on local
fluid chemistry and mineralogy has also been recognized
[Juniper and Tebo, 1995; Karl, 1995], and recent isolation
of vent-related microbes that produce filamentous elemental sulfur [Taylor et al., 1999] and of other microbes that
are actively associated with weathering of extinct sulfides
[Edwards et al., 2003a] has highlighted the importance and
impact that microbial activity has on the geology, geochemistry, and ecology of hydrothermal vent ecosystems at the
seafloor as well as in subseafloor environments.
Over the past two decades, we have gained significant
insights into the diversity and physiology of microbial com-
Deep-sea hydrothermal vents represent one of the most
physically and chemically diverse habitats on Earth for
microbial growth. The geochemical and thermal gradients (e.g., >350°C across distances as small as 1 to 3 cm in
active sulfide chimneys) provide a wide range of niches for
microbial colonization. Psychrophiles, mesophiles, thermophiles, and hyperthermophiles (organisms growing best
1Subground Animalcule Retrieval (SUGAR) Project, Japan Agency
for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
2Department of Biology, Portland State University, Portland, Oregon, USA
Back-Arc Spreading Systems: Geological, Biological, Chemical,
and Physical Interactions
Geophysical Monograph Series 166
Published in 2006 by the American Geophysical Union
10.1029/166GM10
185
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Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
munities associated with these unique ecosystems. Much of
the initial research has focused on mid-ocean ridge (MOR)
systems; recently, however, in light of the greater heterogeneity
of the geochemistry of vent fluids from back-arc basins (BABs),
several studies have begun to explore the linkages between
geochemistry and microbial diversity in these systems.
In this review, we briefly overview methods in microbial
ecology and microbial ecophysiology at vents and discuss the
patterns of diversity (phylogenetic and physiological) that are
emerging from studies in global hydrothermal systems including MOR, BAB, and volcanic arcs (VAs). Because this volume
is dedicated to BABs, the microbiology of MOR systems sets
the stage for comparative studies with BAB systems. Additional
aspects of the microbiology of deep-sea vents and the ecology
of thermophiles are addressed in numerous reviews [Jannasch,
1995; Karl, 1995; Prieur et al., 1995; Huber et al., 2000;
Jeanthon, 2000; Takai and Fujiwara, 2002; Baross et al., 2003,
2004; Cary et al., 2004; Holland et al., 2004; Miroshnichenko,
2004; Takai et al., 2004a; Tivey, 2004].
2. Methods in microbial ecology
in hydrothermal systems
Microbiologists have specific challenges to enumerate
microbial diversity. Unlike most biologists, who can initially
use morphological traits to distinguish new species, microbiologists need to rely on physiological or phylogenetic traits,
and even then, the definition of the microbial species is much
debated. Diversity has traditionally been assessed by culturing
microorganisms. However, recreating the physical and chemical properties of the environment accurately in a culture tube
is rare and frequently results in a culture-biased view of diversity. This bias is particularly a problem for trying to culture
microbes from deep-sea hydrothermal vents, because developing appropriate media and recreating the extreme conditions in
the laboratory are extremely challenging. Consequently, it is
generally accepted that the majority of microorganisms from
vents are not detectable by methods that rely solely on laboratory cultivation. Nevertheless, these approaches have been
crucial in our understanding of the physiological diversity at
deep-sea vents. For example, the upper temperature limits for
life have been challenged by the characterization of Archaea
growing at temperatures above 105°C [Blöchl et al., 1997;
Kashefi et al., 2003], and microbes that use a wide range of
electron donors and acceptors for growth have been described
[Miroshnichenko et al., 2004, for review].
Most of the diversity at deep-sea vents is currently being
described by using molecular phylogeny–based approaches that
circumvent the need to cultivate microbes for assessing microbial diversity [Haddad et al., 1995; Moyer et al., 1995; Polz
and Cavanaugh, 1995; Cary et al., 1997; Takai and Horikoshi,
1999; Reysenbach et al., 2000; Campbell and Cary, 2001; Corre
et al., 2001; Longnecker and Reysenbach, 2001; Takai et al.,
2001; Alain et al., 2002; Lopez-Garcia et al., 2002; Teske et al.,
2002; Hoek et al., 2003; Dhillon et al., 2003; Huber et al., 2003;
Alain et al., 2004; Nakagawa et al., 2004a, 2004b; Higashi et
al., 2004; Takai et al., 2004b, 2004c; Nakagawa et al., 2005a;
Nercessian et al., 2004, 2005]. This approach relies on the
universal and highly conserved small subunit rRNA molecule
(16S rRNA or 18S rRNA), by which all life can be organized
within the domains Bacteria, Archaea, and Eukarya. Cary et
al. [2004] reviewed these molecular phylogenetic approaches
and elaborated more on some of the new advances in molecular
ecological techniques being applied to deep-sea vent microbial communities. Briefly, as illustrated in Figure 1, DNA and
RNA are extracted from environmental samples colonized by
microbes, and the 16S rRNA genes from the genomic DNA and
cDNA assemblages of all microorganisms in the environment
are amplified by polymerase chain reaction (PCR). These products are then sorted by numerous methods such as cloning or
using denaturing gradient gel electrophoresis (DGGE). Unique
clones or bands on the gel, respectively, are sequenced. Using
phylogenetic analysis methods, the sequences can be placed in
a phylogenetic tree or other phylogenetic context. The different sequences (phylotype) represent the range of phylogenetic
diversity in a sample, and their taxonomic position can be
inferred from their closest cultured, known relative. Because
the 16S rRNA gene sequence does not provide information on
the metabolic function or other traits that the microbes might
harbor in the environment, one has to be very careful if making
inferences about the role these organisms play in the environment. In some cases, however, inferences can be made; for
example, if a sequence falls within a lineage that is occupied
only by methanogens, then it is likely that the phylotype can
produce methane. Furthermore, the sequence information can
be used to develop molecular probes and primers that can specifically identify the microorganism in the original sample and
explore the distribution and abundance of the microorganisms
and their rRNA in multiple samples by using fluorescent in situ
hybridization (FISH) and quantitative PCR and hybridization
techniques. Figure 1 illustrates the above processes.
Functional diversity can be explored in a number of different molecular approaches [Cary et al., 2004, for review]
and can be compared to molecular phylogenetic diversity.
The potential metabolic function of a community can be
inferred from detecting genes or mRNA that are diagnostic
for a specific metabolism. For example, a key enzyme for
dissimilatory sulfate reduction, dissimilatory sulfite reductase, is encoded by the dsrAB gene, which has been explored
at deep-sea vents [Cottrell and Cary, 1999; Dhillon et al.,
2003; Hoek et al., 2003; Nakagawa et al., 2004a, 2004b;
Nercessian et al., 2005]. Another frequently examined
Takai et al.
187
Figure 1. Schematic illustration of cultivation-independent, molecular ecological research.
functional gene is the mcrA gene, which encodes an alpha
subunit of methyl coenzyme M reductase, a key enzyme of
methanogenesis; this gene has also been explored at various
deep-sea vents [Dhillon et al., 2005; Nercessian et al., 2005].
More detailed functional diversity can be assessed by using
metagenomic approaches [DeLong, 2002, for review], which
will ultimately shed light on the physiology and ecology of
the as yet largely uncultured diversity at vents.
The next challenge for microbial ecologists is to link the
functional and phylogenetic diversity in situ to biogeochemical
processes. Several methods that may be applied at hydrothermal
vents include stable isotope probing [Radajewski et al., 2000]
and FISH-SIMS [Orphan et al., 2001]. Other potential applications of high-resolution physical and chemical measurements
to molecular biological approaches and microbial ecology will
further enhance our understanding of these systems.
3. Emerging patterns of microbial
diversity in global
hydrothermal systems
3.1. Molecular Phylogenetic Diversity
Initial microbial ecological studies at deep-sea vents were
limited to enrichment culturing or activity measurements
[Jannasch and Wirsen, 1979; Baross et al., 1982; Baross and
Deming, 1983; Jannasch and Wirsen, 1985; Wirsen et al.,
1986]. However, with the development of molecular phylo-
genetic tools for microbial ecology, our view of the microbial
diversity at vents has greatly expanded [for review and examples, see Reysenbach and Shock, 2002; Wilcock et al., 2004].
In most cases, diversity assessments reveal numerous lineages
that still have no known representatives in culture, although
they may provide hints on how to grow novel microbes from
vents. These molecular phylogenetic inventories form the
framework for more in-depth, hypothesis-driven ecological
studies at vents. One can now begin to explore the constraints
(chemical or physical) on the patterns of microbial diversity
at vents and to compare the microbial ecology of BAB hydrothermal systems with that of MOR systems.
3.1.1. Archaea from deep-sea vents. The most comprehensive diversity assessments of deep-sea vents to date have
been limited to the archaeal diversity of communities associated with active chimney structures [e.g., Takai and Horikoshi, 1999; Reysenbach et al., 2000; Corre et al., 2001; Takai
et al., 2001, 2004b, 2004c; Schrenk et al., 2003]. Although
Archaea appear to represent a smaller component (1.8–40%)
of the total cells associated with some sulfide chimneys
[Harmsen et al., 1997; Takai and Horikoshi, 1999; Takai et
al., 2001; Hoek et al., 2003; Schrenk et al., 2003], they do
appear to be important and major components of the diversity in certain portions of chimney structures. For example,
using quantitative fluorogenic PCR and FISH, Takai et al.
[2004c] demonstrated the predominance (nearly 100%) of
Archaea in “in situ colonization systems” (ISCS) and interior
188
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
parts of sulfide chimneys in the Kairei hydrothermal field of
the Central Indian Ridge. Schrenk et al. [2003] showed that
40% of the microorganisms colonizing the exterior wall of
an active sulfide chimney in the Juan de Fuca Ridge were
Archaea, the archaeal proportions increasing steadily toward
the center of the chimney.
These and other studies have led to emerging patterns of
archaeal diversity. In particular, one lineage appears to be
distributed throughout the global deep-sea vent system. Takai
and Horikoshi [1999] referred to this lineage as the “Deepsea Hydrothermal Vent Euryarchaeoic group” (DHVEG).
The lineage is split into DHVE-1 and DHVE-2 [Reysenbach
and Shock, 2002], DHVE-1 being more commonly identified from vents [Takai and Horikoshi, 1999; Reysenbach et
al., 2000; Takai et al., 2001; Longnecker and Reysenbach,
2002; Hoek et al., 2003; Schrenk et al., 2003]. Members of
the DHVEG lineage have formed the majority of clones (up
to 93% of the clones for the DHVE-1) in several archaeal 16S
rDNA chimney clone libraries (Table 1).
Some reports have documented numerous other uncultured archaeal lineages [e.g., Takai and Horikoshi, 1999;
Takai et al., 2001] that included some representatives of
the “Korarchaeota” [Barns et al., 1994] or such unusual
lineages as “Nanoarchaeum” [Hohn et al., 2002; Huber
et al., 2002] (Table 1). Not surprisingly, few members of
cultured representatives are present in the environmental
clone libraries. Among these cultured members, the hyperthermophilic methanogens in the order Methanococcales are
frequently detected [Reysenbach et al., 2000; Teske et al.,
2002; Nercessian et al., 2003; Schrenk et al., 2003; Takai
et al., 2004b, 2004c; Nakagawa et al., 2005a], including
clone libraries obtained from a 2-day deployment of an in
situ enrichment device called the “vent cap” [Reysenbach
et al., 2000] and a 7-day deployment of an ISCS [Takai et
al., 2004c] (Table 1). However, other methanogens belonging to the order Methanosarcinales are often detected in
clone libraries, but they have never been isolated from vents
[Longnecker, 2001; Teske et al., 2002; Schrenk et al., 2003]
(Table 1). The order Thermococcales, which is perhaps the
most frequently cultured group from deep-sea vents [e.g.,
Lepage et al., 2004; Takai et al., 2004c; Nakagawa et al.,
2005a], is not commonly detected in clone libraries, with a
few exceptions [Reysenbach et al., 2000; Teske et al., 2002;
Hoek et al., 2003; Schrenk et al., 2003] (Table 1). Perhaps
in the shallow subsurface environments at vents, complex
community biofilms develop that provide complex organics for the growth of Thermococcales. If this is the case,
then the hyperthermophilic Thermococcales might also be
good indicators of subsurface heterotrophic activity at vents
[Reysenbach et al., 2000; Summit and Baross, 2001; Holland
et al., 2004].
3.1.2. Bacteria from deep-sea vents. Bacteria appear to
dominate most niches at deep-sea vents, the ε-Proteobacteria
being particularly abundant, widespread, and detected in a
variety of habitats, including sulfide structures [Polz and
Cavanaugh, 1995; Hoek et al., 2003; Nakagawa et al., 2004b],
hydrothermal fluid/seawater mixing zones [Reysenbach et al.,
2000; Corre et al., 2001; Huber et al., 2003; Sunamura et al.,
2004; Takai et al., 2004a; Nakagawa et al., 2005d], hydrothermal sediments [Teske et al., 2002], and microbial mats
[Moyer et al., 1995; Longnecker, 2001]. Some ε-Proteobacteria are found in episymbiotic association with deep-sea vent
metazoans [Haddad et al., 1995; Polz and Cavanaugh, 1995;
López-García et al., 2002; Goffredi et al., 2004] (Table 2) and
even as endosymbionts in snails [Suzuki et al., 2005; Urakawa
et al., 2005]. Despite their ubiquitous and cosmopolitan distribution, the physiological aspects of these microorganisms
are poorly understood because of their strong resistance to
cultivation. Previous studies had characterized the ε-Proteobacteria as mostly microaerobic sulfur-oxidizers [Taylor et al.,
1999; López-García et al., 2002]. However, recent culturing
studies have revealed a much greater metabolic diversity of
the ε-Proteobacteria. Recently, numerous representatives of
the deep-sea hydrothermal vent ε-Proteobacteria have been
isolated in pure cultures and characterized [Campbell and
Cary, 2001; Campbell et al., 2001; Alain et al., 2002; Miroshnichenko et al., 2002, 2004; Inagaki et al., 2003, 2004; Takai
et al., 2003a, 2004d, 2005a; Nakagawa et al., 2005a, 2005b,
2005c, 2005d]. These studies indicate that the deep-sea hydrothermal vent ε-Proteobacteria are comprised of mesophilic
to moderately thermophilic chemolitho- autotrophs capable
of oxidizing hydrogen and sulfur compounds with nitrate,
oxygen, and sulfur compounds as terminal electron acceptors
[Campbell and Cary, 2001; Alain et al., 2002; Miroshnichenko
et al., 2002, 2004; Inagaki et al., 2003, 2004; Takai et al.,
2003a, 2004d, 2005a; Nakagawa et al., 2005a, 2005b, 2005c,
2005d]. It is now well accepted that the ε-Proteobacteria play
a significant role not only in the cycling of sulfur, but also
in the cycling of hydrogen, nitrogen, and carbon in deep-sea
hydrothermal environments [Takai et al., 2003a; Nakagawa
et al., 2005b, 2005c].
Another group of chemolithoautotrophs is represented by
members of the order Aquificales, which utilize similar electron donor/acceptor pairs as the ε-Proteobacteria [Götz et al.,
2002; Nakagawa et al., 2003]. Like the ε-Proteobacteria, the
Aquificales are found in globally widespread deep-sea hydrothermal fields [Reysenbach et al., 2000; Nakagawa et al., 2003,
2004b; Takai et al., 2003b] (Table 2). As predicted from the high
growth temperatures of the Aquificales, these microorganisms
are found only in high-temperature habitats such as active sulfide structures and vent fluids [Reysenbach et al., 2002; Takai
et al., 2003b; Nakagawa et al., 2004b, 2005a].
Takai et al.
Table 1. Summary of phylogenetic diversity of archaeal rRNA gene clones in deep-sea hydrothermal environments.
Group
Euryarchaeota
Archaeoglobales
Location
Habitat
References
In situ growth chamber
Reysenbach et al., 2000
Chimney
Schrenk et al., 2003
In situ growth chamber
Nercessian et al., 2003
In situ colonization device and
chimney
Hydrothermal sediments
Takai et al., 2004c
In situ growth chamber
Higashi et al., 2004
Chimney
Nakagawa et al., 2005a
In situ growth chamber
Reysenbach et al., 2000
Chimney
Schrenk et al., 2003
In situ growth chamber
Nercessian et al., 2003
In situ colonization device and
chimney
Hydrothermal plume
Sulfide spire
Hydrothermal sediments
Takai et al., 2004c
In situ growth chamber
Higashi et al., 2004
Sulfur chimney
Nakagawa et al., 2006
Chimney
Takai et al., 2001
In situ colonization device and
chimney
Nakagawa et al., 2005a
Chimney
Schrenk et al., 2003
In situ growth chamber
Nercessian et al., 2003
Takai et al., 2004c
Guaymas Basin (MOR)
Manus Basin (BAB)
PACMANUS
Okinawa Trough (BAB)
Iheya North
In situ colonization device and
chimney
Hydrothermal sediments
Chimney
Takai et al., 2001
In situ colonization device and
chimney
Nakagawa et al., 2005a
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Mothra
NEPR (MOR)
13°N
CIR (MOR)
Kairei
Guaymas Basin (MOR)
Izu-Bonin Arc (VA)
Suiyo Seamount
Okinawa Trough (BAB)
Iheya North
Teske et al., 2002
Thermococcales
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Mothra
NEPR (MOR)
13°N
CIR (MOR)
Kairei
Edmond
Guaymas Basin (MOR)
Izu-Bonin Arc (VA)
Suiyo Seamount
Mariana Arc (VA)
TOTO Caldera
Manus Basin (BAB)
PACMANUS
Okinawa Trough (BAB)
Iheya North
Methanococcales
Juan de Fuca (MOR)
Mothra
NEPR (MOR)
13°N
CIR (MOR)
Kairei
Methanobacteriales
Takai et al., 2004b
Hoek et al., 2003
Teske et al., 2002
Teske et al., 2002
189
190
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Table 1. Cont.
Group
ANME-1
Location
Habitat
References
Guaymas Basin (MOR)
Okinawa Trough (BAB)
Iheya Ridge
Hydrothermal sediments
Teske et al., 2002
Hydrothermal sediments
Takai and Horikoshi, 1999
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002
Juan de Fuca (MOR)
Mothra
Guaymas Basin (MOR)
Chimney
Hydrothermal sediments
Schrenk et al., 2003
Teske et al., 2002
In situ colonization device and
chimney
Takai et al., 2004c
In situ growth chamber
Nercessian et al., 2003
In situ colonization device and
chimney
Hydrothermal plume
Takai et al., 2004c
Chimney
Takai et al., 2001
In situ growth chamber
Reysenbach et al., 2000
Chimney
Schrenk et al., 2003
In situ growth chamber
Nercessian et al., 2003
Chimney
Hydrothermal sediments
Takai et al., 2004c
Teske et al., 2002
Chimney
Takai et al., 2001
Chimney
Takai and Horikoshi, 1999
In situ growth chamber
Reysenbach et al., 2000
In situ growth chamber
Nercessian et al., 2003
Sulphide spire (diffuse flow)
Hoek et al., 2003
In situ growth chamber
Chimney
Chimney
Higashi et al., 2004
Takai and Horikoshi, 1999
Takai and Horikoshi, 1999
Sulfur chimney
Nakagawa et al., 2006
Methanomicrobiales
Methanosarcinales
ANME-2
Methanosarcina
CIR (MOR)
Kairei
Methanopyrales
NEPR (MOR)
13°N
CIR (MOR)
Kairei
Takai et al., 2004b
Halobacteriales
Manus Basin (BAB)
PACMANUS
DHVEG
DHVEG-1 (Marine Benthic Group D)
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Mothra
NEPR (MOR)
13°N
CIR (MOR)
Kairei
Guaymas Basin (MOR)
Manus Basin (BAB)
PACMANUS
Izu-Bonin Arc (VA)
Myojin Knoll
DHVEG-2
MAR (MOR)
Snake Pit
NEPR (MOR)
13°N
CIR (MOR)
Edmond
Izu-Bonin Arc (VA)
Suiyo Seamount
Myojin Knoll
Mariana Arc (VA)
TOTO Caldera
Takai et al.
Table 1. Cont.
Group
DHVEG II
DHVEG-3, 4, 5, 6, 8
Location
Okinawa Trough (BAB)
Iheya Ridge
Iheya North
NEPR (MOR)
13°N
Juan de Fuca (MOR)
Mothra
Izu-Bonin Arc (VA)
Myojin Knoll
Okinawa Trough (BAB)
Iheya Ridge
Iheya North
Habitat
References
Hydrothermal sediments
In situ colonization device
Takai and Horikoshi, 1999
Nakagawa et al., 2005a
In situ growth chamber
Nercessian et al., 2003
Chimney
Schrenk et al., 2003
Chimney
Takai and Horikoshi, 1999
Hydrothermal sediments
In situ colonization device
Takai and Horikoshi, 1999
Nakagawa et al., 2005a
Hydrothermal plume
Huber et al., 2003
In situ colonization device and
chimney
Hydrothermal plume
Takai et al., 2004c
Microbial mat
Moyer et al., 1998
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ colonization device and
chimney
Takai et al., 2004c
In situ growth chamber
Nercessian et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
Chimney
Takai et al., 2001
Sulfur chimney
Nakagawa et al., 2006
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ growth chamber
Nercessian et al., 2003
Hydrothermal plume
Chimney
Huber et al., 2003
Schrenk et al., 2003
In situ colonization device and
chimney
Hydrothermal plume
Takai et al., 2004c
Chimney
Takai and Horikoshi, 1999
Marine Group II
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
Loihi Seamount (hot spot)
PeleÅfs vent
Okinawa Trough (BAB)
Iheya North
Marine Benthic Group E
CIR (MOR)
Kairei
Crenarchaeota
Desulfurococcales
NEPR (MOR)
13°N
CIR (MOR)
Karai
Manus Basin (BAB)
PACMANUS
Mariana Arc (VA)
TOTO Caldera
Okinawa Trough (BAB)
Iheya North
Marine Group I
NEPR (MOR)
13°N
Juan de Fuca (MOR)
Axial volcano
Mothra
CIR (MOR)
Kairei
Izu-Bonin Arc (VA)
Myojin Knoll
Takai et al., 2004b
Takai et al., 2004b
191
192
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Table 1. Cont.
Group
Location
Okinawa Trough (BAB)
Iheya North
Loihi Seamount (hot spot)
PeleÅfs vent
Habitat
References
Vent fluid
In situ colonization device and
chimney
Takai and Horikoshi, 1999
Nakagawa et al., 2005a
Microbial mat
Moyer et al., 1998
In situ growth chamber
Hydrothermal sediments
Reysenbach et al., 2000
Teske et al., 2002
Chimney
Takai et al., 2001
Chimney
Chimney
Takai and Horikoshi, 1999
Takai and Horikoshi, 1999
In situ colonization device and
chimney
Nakagawa et al., 2005a
Hydrothermal sediments
Teske et al., 2002
Chimney
Schrenk et al., 2003
Hydrothermal sediments
Chimney
Takai and Horikoshi, 1999
Nakagawa et al., 2005a
In situ growth chamber
Nercessian et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
Chimney
Nakagawa et al., 2005a
Chimney
Nakagawa et al., 2004b
Marine Benthic Group B
(DHVCG-I, SAG, MHVG1-3)
MAR (MOR)
Snake Pit
Guaymas Basin (MOR)
Manus Basin (BAB)
PACMANUS
Izu-Bonin Arc (VA)
Suiyo seamount
Myojin Knoll
Okinawa Trough (BAB)
Iheya North
Marine Pelagic Arch Group I
Guaymas Basin (MOR)
Hot Water Crenarchaeota
Group (HWCG)
Juan de Fuca (MOR)
Mothra
Okinawa Trough (BAB)
Iheya Ridge
Iheya North
Korarchaeota
NEPR (MOR)
13°N
CIR (MOR)
Kairei
Okinawa Trough (BAB)
Iheya North
Nanoarchaeota
Izu-Bonin Arc (VA)
Suiyo Seamount
Bacterial diversity at deep-sea vents spans most of
the known, nonphotosynthetic lineages, including the
Firmicutes, the Verrucomicrobia, the Thermales, and the
Cytophaga–Flexibacter–Bacteroides (CFB) group (Table 2).
The Verrucomicrobia have been detected at numerous hydrothermal sites [Alain et al., 2002; Lopez-Garcia et al., 2002;
Teske et al., 2002] on the Juan de Fuca Ridge, Northern East
Pacific Rise, and Guaymas Basin (Table 2). This group of
organisms has been difficult to grow from most environments; enrichment cultures growing on complex organic
media at 70°C were gradually selected for a new verrucomicrobial strain, but the strain could not be retrieved later
from the culture collection storage [A.-L. Reysenbach and
D. Götz, unpublished data, 2000].
Another bacterial group also detected in several clone
libraries from deep-sea hydrothermal vent environments
is the green nonsulfur bacteria, presently designated as
the phylum Chloroflexi [Alain et al., 2002; Teske et al.,
2002; Dhillon et al., 2003; Goffredi et al., 2004] (Table 2).
Based on the phylogenetic tree inferred from 16S rRNA gene
sequences [Hugenholtz et al., 1998], the phylum Chloroflexi
is divided into four subphyla. Of these, Subphylum III comprises the cultured representatives of a wide range of phenotypes, including thermophilic phototrophic bacteria from
terrestrial hot springs, such as Chloroflexus aurantiacus and
Herpetosiphon geysericola. Other than Subphylum III, there
are very limited cultured representatives of the nonphotosynthetic members. The anaerobic dechlorinating bacterium
Takai et al.
Dehalococcoides dehalogenes is the only cultivated representative within the Subphylum II, growing by the oxidation
of hydrogen and dechlorination of tetrachlorethene to ethane
[Maymo-Gatell et al., 1997]. Anaerolinea thermophila and
Caldilinea aerophila are thermophilic chemorogantrophs
of Subphylum I, isolated from thermophilic granular sludge
and microbial mats in a hot spring, respectively [Sekiguchi
et al., 2003]. The habitat preferences of nonphotosynthetic
green nonsulfur bacteria are compatible with the geochemical features of sediment-hosted hydrothermal systems, such
as the Guaymas Basin, where organic biomass undergoes
pyrolysis and thermal alteration to a wide variety of petroleum hydrocarbons, including unbranched alkanes, cycloalkanes, triterpanes, steranes and diasteranes, and aromatic
hydrocarbons [Teske et al. 2002].
Recently, several studies have explored the diversity of dissimilatory sulfate-reducing bacteria (SRB) at deep-sea vents
by using a functional gene approach [Dhillon et al., 2003;
Hoek et al., 2003; Nakagawa et al., 2004a, 2004b] (Table 3).
These studies, which used the dsrAB gene, have expanded
our view of the distribution and diversity of SRB at vents
and show a diverse assemblage of sulfate reducers not only
in hydrothermal sediments of the Guaymas Basin but also
in the walls of actively venting sulfide chimneys. In addition, the molecular phylogenetic surveys of the dsrAB gene
have demonstrated the existence of previously uncultivated
and unidentified groups of potential SRB, designated as
“functional gene-only” groups of SRB [Dhillon et al., 2003;
Nakagawa et al., 2004a, 2004b]. It has been suggested that
these sulfate-reducers can have a significant impact on the
chemistry and mineralogy of local microenvironments and
may play a role in the precipitation and alteration of sulfide
minerals in deep-sea vent ecosystems [Shanks, 2001]. To
begin to address the potential geobiological role of sulfatereducers in deep-sea vents, J. Hoek and A.-L. Reysenbach
[unpublished data, 2003] explored how a thermophilic, H2oxidizing, chemolithoautotrophic sulfate-reducing bacterium
fractionated sulfur isotopes under the steep geochemical
gradients of sulfide chimneys. The extent of fractionation
was strongly dependent on the concentration of H 2 in the
environment; where H2 limited growth, sulfide was depleted
in 34S by up to ~40‰ from the original sulfate. This reduction suggests that sulfide minerals derived from the sulfide
of chemolithoautotrophic SRB can be detected from the
isotopic signature of sulfur, which is potentially an important
tool for studying the impact of sulfate-reducing prokaryotes
on biogeochemical cycling in deep-sea vents.
Metal oxidizers such as iron-oxidizing Bacteria are important contributors to microbial weathering of extinct sulfides
and can have a significant impact on the biogeochemical
cycling of metals and sulfur at deep-sea vents [Edwards et
193
al., 2003a, 2003b]. McCollum and Shock [1997] estimated
that the amount of energy available from the oxidation of
metal sulfide minerals precipitated from a seafloor hydrothermal plume exceeded the energy available from dissolved
compounds (H 2S, CH4, Mn 2+, H 2) by nearly an order of
magnitude per kilogram of vent fluid. Edwards et al. [2003a]
examined the role of iron-oxidizing Bacteria in the oxidation
of ferrous iron (Fe2+) from sulfide minerals as an energy
source in seafloor environments. Polished slabs of chimney
sulfides, when incubated on the seafloor at ambient temperatures (~4°C), were heavily colonized, and colony density
showed a positive correlation with the solubility of the mineral substrate. The observation of concomitant formation of
Fe-oxide on the chimney slabs suggests that the Fe-oxides
formed in situ during bacterial growth. Further support for
the presence and activity of iron-oxidizing Bacteria associated with seafloor hydrothermal vent sulfides comes from
the isolation of iron-oxidizing Bacteria from the in situ incubation experiments of Edwards et al. [2003a]. Phylogenetic
characterization of these isolates revealed a diverse collection
of α- and γ-Proteobacteria, which were not closely related to
any known iron-oxidizing Bacteria [Edwards et al., 2003b].
These results suggest that iron-oxidizing Bacteria are prevalent and active at seafloor hydrothermal sulfide habitats.
3.2. Microbial Physiological Diversity at Deep-Sea Vents
Some of the diversity described above represents the range
of physiological diversity at vents—from mesophiles to thermophiles, from obligate chemolithoautotrophs to facultative
heterotrophs—and includes anaerobes, microaerophiles, and
aerobes. This diversity is supported by the steep chemical
and physical gradients typical of deep-sea hydrothermal
environments. These steep gradients generate a wide range
of niches and energy sources for microorganisms. For example, chemolithoautotrophs can generate energy by exploiting
the chemical disequilibria resulting from sluggish reaction
kinetics for redox reactions at the interface between oxidized
seawater (e.g., O2, NO3 –, and SO42–) and reduced hydrothermal vent fluids (e.g., H2, H2S, CH4, CO2, and formate).
Although a range of novel chemolithoautotrophs have been
isolated from deep-sea vents [Jannasch, 1995; Karl, 1995;
Prieur et al., 1995; Huber et al., 2000; Jeanthon, 2000; Takai
and Fujiwara, 2002; Miroshnichenko et al., 2004], many
more remain uncultured, perhaps including some that use
rare or unusual redox couples (Table 4) [Shock and Holland,
2004]. Although not all of these processes are microbiologically mediated at high temperatures, microniches likely
exist where thermophiles capitalize on the mixing between
cold oxygenated seawater and reduced hydrothermal vent
fluid. Microbes that are able to use multiple electron donors
194
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Table 2. Summary of phylogenetic diversity of bacterial rRNA gene clones in deep-sea hydrothermal environments.
Group
ε-Proteobacteria
Subgroup A
Location
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
Okinawa Trough (BAB)
Iheya North
Subgroup B
MAR (MOR)
Snake Pit
Rainbow
Juan de Fuca (MOR)
Axial Volcano
NEPR (MOR)
13°N
Guaymas Basin (MOR)
CIR (MOR)
Kairei
Loihi Seamount (Hot Spot)
Pele’s vent
Izu-Bonin Arc (VA)
Suiyo Seamount
Mariana Arc (VA)
TOTO caldera
Okinawa Trough (BAB)
Iheya North
Subgroup C
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
Subgroup D
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
13°N
SEPR (MOR)
17°S
Habitat
References
In situ growth chamber
Corre et al., 2001
Paralvinella tube
Alain et al., 2002
In situ colonization device and
chimney
Takai et al., 2004c
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ growth chamber
In situ growth chamber
In situ growth chamber
Corre et al., 2001
Reysenbach et al., 2000
Lopez-Garcia et al., 2003
Hydrothermal Plume
Paralvinella tube
Huber et al., 2003
Alain et al., 2002
In situ growth chamber
Hydrothermal sediments
Alain et al., 2004
Teske et al., 2002;
Dhillon et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
Microbial mat
Moyer et al., 1995
In situ growth chamber
Higashi et al., 2004
Sulfur chimney
Nakagawa et al., 2006
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ growth chamber
Corre et al., 2001
Hydrothermal plume
Huber et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
In situ growth chamber
In situ growth chamber
Corre et al., 2001
Reysenbach et al., 2000
Hydrothermal plume
Huber et al., 2003
In situ growth chamber
Alain et al., 2004
Chimney
Longnecker and Reysenbach,
2001
Takai et al.
Table 2. Cont.
Group
Location
CIR (MOR)
Edmond
Kairei
Izu-Bonin Arc (VA)
Suiyo Sea-Mount
Mariana Arc (VA)
TOTO caldera
Okinawa Trough (BAB)
Iheya North
Subgroup E (Sulfurospirillum Group)
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
13°N
CIR (MOR)
Edmond
Kairei
Okinawa Trough (BAB)
Iheya North
Subgroup F
MAR (MOR)
Snake Pit
Rainbow
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
13°N
9°N
CIR (MOR)
Edmond
Kairei
Guaymas Basin (MOR)
Izu-Bonin Arc (VA)
Suiyo Seamount
Okinawa Trough (BAB)
Iheya North
Subgroup G
MAR (MOR)
Snake Pit
Habitat
References
Sulphide spire
In situ colonization device and
chimney
Hoek et al., 2003
Takai et al., 2004c
In situ growth chamber
Higashi et al., 2004
Sulfur chimney
Nakagawa et al., 2006
In situ colonization device
Nakagawa et al., 2005a
In situ growth chamber
Corre et al., 2001
Paralvinella tube
Alain et al., 2002
In situ growth chambers
Alain et al., 2004
Sulphide spire diffuse flow
In situ colonization device and
chimney
Scaly snail (Crysomallon
squamiferum)
Hoek et al., 2003
Takai et al., 2004c
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ growth chamber
In situ growth chamber
Hydrothermal sediments
In situ growth chamber
Corre et al., 2001
Reysenbach et al., 2000
Lopez-Garcia et al., 2003
Lopez-Garcia et al., 2003
Hydrothermal plume
Paralvinella tube
Huber et al., 2003
Alain et al., 2002
A. pompejana epibiont
In situ growth chambers
R. pachyptila tube
Haddad et al., 1995
Alain et al., 2004
Lopez-Garcia et al., 2002
Sulphide spire diffuse flow
In situ colonization device and
chimney
Scaly snail (Crysomallon
squamiferum)
Hydrothermal sediments
Hoek et al., 2003
Takai et al., 2004c
Hydrothermal plume
Sunamura et al., 2004
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ growth chamber
Corre et al., 2000
Goffredi et al., 2004
Goffredi et al., 2004
Teske et al., 2002;
Dhillon et al., 2003
195
196
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Table 2. Cont.
Group
Location
Juan de Fuca (MOR)
Axial volcano
SEPR (MOR)
17°S
CIR (MOR)
Kairei
Mariana Arc (VA)
TOTO caldera
Okinawa Trough (BAB)
Iheya North
Arcobacter Group
MAR (MOR)
Rainbow
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
13°N
CIR (MOR)
Kairei
α-Proteobacteria
MAR (MOR)
Rainbow
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
9°N
CIR (MOR)
Kairei
β-Proteobacteria
Izu-Bonin Arc (VA)
Suiyo Seamount
Okinawa Trough (BAB)
Iheya North
MAR (MOR)
Rainbow
Snake Pit
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
γ-Proteobacteria
MAR (MOR)
Rainbow
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
Habitat
References
Hydrothermal plume
Huber et al., 2003
Chimney
Longnecker and Reysenbach,
2001
In situ colonization device and
chimney
Takai et al., 2004c
Sulfur chimney
In situ colonization device and
chimney
Nakagawa et al., 2006
Nakagawa et al., 2005a
In situ growth chamber
Lopez-Garcia et al., 2003
Hydrothermal plume
Huber et al., 2003
In situ growth chambers
Alain et al., 2004
In situ colonization device and
chimney
Takai et al., 2004c
Hydrothermal sediments
Lopez-Garcia et al., 2003
Hydrothermal plume
Huber et al., 2003
R. pachyptila tube
Lopez-Garcia et al., 2002
In situ colonization device and
chimney
Takai et al., 2004c
In situ growth chamber
Higashi et al., 2004
In situ colonization device
Nakagawa et al., 2005a
Hydrothermal sediments
In situ growth chamber
Lopez-Garcia et al., 2003
Reysenbach et al., 2000
Hydrothermal plume
Huber et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
Hydrothermal sediments
Lopez-Garcia et al., 2003
Hydrothermal plume
Paralvinella tube
Huber et al., 2003
Alain et al., 2002
Takai et al.
Table 2. Cont.
Group
Location
9°N
13°N
CIR (MOR)
Kairei
Habitat
R. pachyptila tube
In situ growth chambers
References
Lopez-Garcia et al., 2002
Alain et al., 2004
In situ colonization device and
chimney
Scaly snail (Crysomallon
squamiferum)
Microbial mat
Takai et al., 2004c
Hydrothermal plume
Sunamura et al., 2004
Sulfur chimney
Nakagawa et al., 2006
In situ colonization device and
chimney
Nakagawa et al., 2005a
Paralvinella tube
Alain et al., 2002
In situ colonization device and
chimney
Scaly snail (Crysomallon
squamiferum)
Takai et al., 2004c
In situ colonization device and
chimney
Nakagawa et al., 2005a
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002; Dhillon et
al., 2003
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002
MAR (MOR)
Rainbow
Guaymas Basin (MOR)
Loihi Seamount (hot spot)
Hydrothermal sediments
Hydrothermal sediments
Microbial mat
Lopez-Garcia et al., 2003
Teske et al., 2002
Moyer et al., 1995
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002
In situ growth chamber
Hydrothermal sediments
In situ growth chamber
Reysenbach et al., 2000
Lopez-Garcia et al., 2003
Lopez-Garcia et al., 2003
Paralvinella tube
Hydrothermal sediments
Alain et al., 2002
Teske et al., 2002; Dhillon et
al., 2003
R. pachyptila tube
In situ growth chamber
Lopez-Garcia et al., 2002
Alain et al., 2004
In situ colonization device and
chimney
Takai et al., 2004c
Loihi Seamount (hot spot)
Izu-Bonin Arc (VA)
Suiyo Seamount
Mariana Arc (VA)
TOTO caldera
Okinawa Trough (BAB)
Iheya North
δ-Proteobacteria
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
Okinawa Trough (BAB)
Iheya North
Desulfobacterium
Desulfobulbus
Goffredi et al., 2004
Moyer et al., 1995
Goffredi et al., 2004
Myxobacteria
Geobacter
CFB Group
MAR (MOR)
Snake Pit
Rainbow
Juan de Fuca (MOR)
Axial volcano
Guaymas Basin (MOR)
NEPR (MOR)
9°N
13°N
CIR (MOR)
Kairei
197
198
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Table 2. Cont.
Group
Location
Okinawa Trough (BAB)
Iheya North
Green Nonsulfur Group
(Chloroflexi)
Juan de Fuca (MOR)
Axial volcano
Guaymas Basin (MOR)
CIR (MOR)
Kairei
Okinawa Trough (BAB)
Iheya North
Desulfurobacterium Group
MAR (MOR)
Snake Pit
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
Thermodesulfobacterium Group
Juan de Fuca (MOR)
Axial volcano
CIR (MOR)
Kairei
Okinawa Trough (BAB)
Iheya North
Habitat
Scaly snail (Crysomallon
squamiferum)
References
Goffredi et al., 2004
In situ colonization device and
chimney
Nakagawa et al., 2005a
Paralvinella tube
Hydrothermal sediment
Alain et al., 2002
Teske et al., 2002; Dhillon et
al., 2003
Scaly snail (Crysomallon
squamiferum)
Goffredi et al., 2004
In situ colonization device and
chimney
Nakagawa et al., 2005a
In situ growth chamber
Reysenbach et al., 2000
Hydrothermal plume
Huber et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
Hydrothermal plume
Huber et al., 2003
In situ colonization device and
chimney
Takai et al., 2004c
Chimney
Nakagawa et al., 2005a
In situ growth chamber
Reysenbach et al., 2000
Sulphide spire diffuse flow
In situ colonization device and
chimney
Hoek et al., 2003
Takai et al., 2004c
Chimney
Nakagawa et al., 2005a
Paralvinella tube
Alain et al., 2002
R. pachyptila tube
Hydrothermal sediments
Lopez-Garcia et al., 2002
Teske et al., 2002
Hydrothermal sediments
Hydrothermal sediments
Lopez-Garcia et al., 2003
Teske et al., 2002
Chimney
Nakagawa et al., 2005a
Hydrothermal sediments
Teske et al., 2002
Aquificales
MAR (MOR)
Snake Pit
CIR (MOR)
Edmond
Kairei
Okinawa Trough (BAB)
Iheya North
Verucomicrobia
Juan de Fuca (MOR)
Axial volcano
NEPR (MOR)
9°N
Guaymas Basin (MOR)
Planctomycetales
MAR (MOR)
Rainbow
Guaymas Basin (MOR)
Okinawa Trough (BAB)
Iheya North
Cyanobacteria and Chloroplasts
Guaymas Basin (MOR)
Takai et al.
199
Table 2. Cont.
Group
Firmicutes
Location
Juan de Fuca (MOR)
Axial volcano
Habitat
References
Hydrothermal plume
Paralvinella tube
Hydrothermal sediment
13°N
MAR (MOR)
Rainbow
In situ growth chamber
Huber et al., 2003
Alain et al., 2002
Teske et al., 2002; Dhillon et
al., 2003
Alain et al., 2004
Hydrothermal sediments
Lopez-Garcia et al., 2003
NEPR (MOR)
Guaymas Basin (MOR)
A. pompejana epibionts
Hydrothermal sediments
Campbell and Cary, 2001
Teske et al., 2002
Hydrothermal sediments
Lopez-Garcia et al., 2003
Chimney
Nakagawa et al., 2005a
R. pachyptila tube
Hydrothermal sediments
Lopez-Garcia et al., 2002
Teske et al., 2002; Dhillon et
al., 2003
Guaymas Basin (MOR)
Okinawa Trough (BAB)
Iheya North
Hydrothermal sediments
Teske et al., 2002
Chimney
Nakagawa et al., 2005a
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002, Dhillon et
al., 2003
Guaymas Basin (MOR)
Hydrothermal sediments
Teske et al., 2002, Dhillon et
al., 2003
Guaymas Basin (MOR)
Okinawa Trough (BAB)
Iheya North
Hydrothermal sediments
Teske et al., 2002
In situ colonization device
Nakagawa et al., 2005a
Guaymas Basin (MOR)
Spirochetes
Nitrospira Group
Thermus/Deinococcus Group
OP8 candidate division
MAR (MOR)
Rainbow
Okinawa Trough (BAB)
Iheya North
NEPR (MOR)
9°N
Guaymas Basin (MOR)
OP1 candidate division
OP3 candidate division
OP5 candidate division
OP9 candidate division
OP11 candidate division
and acceptors are best suited for these fluctuating environments and steep gradients. Thus, these Bacteria can also
occupy suboxic zones where NO3–, S2O32–, Fe3+, and Mn4+ are
the oxidizing agents instead of O2. Many vent thermophiles
show a metabolic versatility that may reflect their ability to
thrive in environments where the geochemical gradients are
fluctuating, including the facultative aerobic obligate chemolithotroph Pyrolobus fumarii [Blöchl et al., 1997], members
of Aquificales [Götz et al., 2002; Nakagawa et al., 2003], the
Desulfurobacteria group [L’Haridon et al., 1998; Alain et al.,
2003; Takai et al., 2003b], and ε-Proteobacteria [Campbell and
Cary, 2001; Alain et al., 2002; Miroshnichenko et al., 2002,
2004; Inagaki et al., 2003, 2004; Takai et al., 2003a, 2004d,
2005a; Nakagawa et al., 2005a, 2005b, 2005c, 2005d].
Although calculations of thermodynamic free energy from
redox reactions can be used as proxies for metabolic potential, they can be misleading if kinetic inhibition of certain
chemical reactions under different conditions as well as competition and bioavailability of electron donors and acceptors
in the natural environment are not considered. Thus, modeling efforts that take into account the different constraints
on biological activity provide a framework for exploring
novel physiologies and metabolisms. Tivey [2004] estimated
environmental conditions (temperature, chemistry, and pH)
within chimneys and flanges of seafloor vent deposits by
developing models that account for rates of fluid flow, diffusive and advective transport of seawater and end-member
fluid across chimney walls, the composition and temperature
200
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Table 3. Diversity of dsrAB and mcrA gene clones in deep-sea hydrothermal environments.
Group
Location
Habitat
References
Chimney
Nakagawa et al., 2004a
Hydrothermal sediments
Dhillon et al., 2003
Chimney
Nakagawa et al., 2004a
Chimney and in situ sampler
Nercessian et al., 2004
Guaymas Basin (MOR)
Hydrothermal sediments
Dhillon et al., 2003
Guaymas Basin (MOR)
Hydrothermal sediments
Dhillon et al., 2003
Chimney
Nakagawa et al., 2004a
Chimney and in situ sampler
Nercessian et al., 2004
Hydrothermal sediments
Nercessian et al., 2004
Chimney
Nakagawa et al., 2004a
In situ growth chamber
Nakagawa et al., 2004b
Chimney
Nakagawa et al., 2004a
Chimney and in situ sampler
Nercessian et al., 2004
Chimney
Nakagawa et al., 2004a
Suiyo Seamount
In situ growth chamber
Nakagawa et al., 2004b
Guaymas Basin (MOR)
Hydrothermal sediments
Dhillon et al., 2003
In situ growth chamber
Nakagawa et al., 2004b
In-situ sampler
Nercessian et al., 2004
Hydrothermal sediments
Nercessian et al., 2004
dsrAB
Iheya North group (group I)
Okinawa Trough (BAB)
Iheya North
Guaymas group (group IV)
Guaymas Basin (MOR)
Archaeoglobaceae
CIR (MOR)
Kairei
NEPR (MOR)
13 ˚N
Syntrophobacterales
Gram-positive SRB relatives
Desulfoarculus-relatives
Okinawa Trough (BAB)
Iheya North
Desulfobulbaceae-relatives
NEPR (MOR)
13 ˚N
MAR (MOR)
Rainbow
Okinawa Trough (BAB)
Iheya North
Izu-Bonin Arc (VA)
Suiyo Seamount
Thermodesulfobacteria-relatives
CIR (MOR)
Kairei
NEPR (MOR)
13 ˚N
Okinawa Trough (BAB)
Iheya North
Izu-Bonin Arc (VA)
Desulfobacteraceae
Izu-Bonin Arc (VA)
Suiyo Seamount
mcrA
Methanopyrales
NEPR (MOR)
13˚N
MAR (MOR)
Rainbow
Methanococcales
MAR (MOR)
Rainbow
Chimney
Nercessian et al., 2004
Hydrothermal sediments
Dhillon et al., 2005
Rainbow
Guaymas Basin (MOR)
Hydrothermal sediments
Hydrothermal sediments
Nercessian et al., 2004
Dhillon et al., 2005
Guaymas Basin (MOR)
Hydrothermal sediments
Dhillon et al., 2005
Guaymas Basin (MOR)
Methanosarcinales-relatives
MAR (MOR)
Methanomicrobiales-relatives
Takai et al.
of ambient seawater and end-member vent fluid, and the
physical configuration (pore size and mineral distribution)
of single-walled vent structures. Results from these modeling
efforts indicate that the pH and oxidation state of pore fluids
across chimney walls are highly sensitive to the composition
of the end-member fluid and to different styles of mixing.
The temperature of the transition from oxidized to reduced
conditions varied from <3°C to ~90°C. According to the
model, metabolic energy available to microorganisms within
the vent structures is largely a function of the oxidation state
of the pore fluid. Furthermore, the pH of pore fluids at temperatures of 80°C to 120°C is generally low (pH < 3–4.5),
suggesting that actively venting chimneys may harbor as yet
uncultivated thermophilic, anaerobic acidophiles.
Patterns of inorganic carbon assimilation are quite diverse
in vent environments and might be strongly associated with
local physical and chemical conditions coupled with the
inorganic carbon flow. Hyperthermophilic Euryarchaeota,
such as methanogens and Archaeoglobales members,
frequently colonize in the highest temperature ranges of
habitats and utilize the acetyl-CoA pathway for their autotrophic CO2 fixation [Fuchs, 1990, 1994; Vorholt et al., 1995,
1997]. In contrast, the carbon fixation pathways of members of Desulfurococcales such as Pyrolobus, Pyrodictium,
Desulfurococcus, and Ignicoccus, which are hyperthermophilic Crenarchaeota dwelling in deep-sea hydrothermal vent
environments, are still uncertain, but the modified Calvin
cycle and a potentially new carbon fixation pathway have
been suggested after enzymatic analyses for Pyrodictiaceae
201
and Desulfurococcaceae, respectively [Hügler et al., 2003].
In the lower temperatures of mixing zones, it has been demonstrated that marine Crenarchaeota group I (MGI) represents the most abundant archaeal components [Moyer et al.,
1998; Takai et al., 2004b]. Stable and radiocarbon isotopic
analyses of archaeal membrane lipids (glycerol dibiphytanyl
glycerol tetraethers) have suggested that these previously
uncultivated MGI members can grow autotrophically by
bicarbonate fixation via a 3-hydroxypropionate pathway
[Pearson et al., 2001; Wuchter et al., 2003]. In the bacterial components, the reductive tricarboxylic acid (rTCA)
cycle is probably one of the most predominant CO2 fixation
pathways operated by Aquifex and Persephonella, members
of Aquificales [Zhang et al., 2002]. In addition, several
molecular phylogenetic analyses of key functional genes for
autotrophic carbon fixation pathways and enzymatic analyses using deep-sea ε-Proteobacteria and γ-Proteobacteria
isolates have demonstrated that the rTCA cycle can serve
as a CO2 fixation pathway of deep-sea ε-Proteobacteria and
contribute to the primary production of the microbial community together with the Calvin cycle by γ-Proteobacteria in
the mixing zones [Campbell et al., 2003; Campbell and Cary,
2004; Hügler et al., 2005; Takai et al., 2005b].
Tolerance of steep physical and chemical gradients is an
important physiological characteristic of microorganisms
in deep-sea vent environments. The effects of temperature
and hydrostatic pressure at in situ habitats on the survivial
of heterotrophic hyperthermophiles have been studied extensively [Trent et al., 1990; Holden and Baross, 1993, 1995;
Table 4. Range of energetically favorable redox reactions available to chemolithotrophic microorganisms in deep-sea hydrothermal vents.
Type of metabolism
Methanotrophy
Methanotrophy
Methanogenesis
S reduction (sulfate reduction)
S reduction (sulfur reduction)
S oxidation
S oxidation
S oxidation
S oxidation/dentrification
S oxidation/denitrification
S oxidation/denitrification
H2 oxidation
Fe reduction
Fe oxidation
Fe oxidation/denitrification
Mn reduction
Nitrification
Nitrification
Denitrification
Electron
donor
CH4
CH4
H2
H2
H2
H 2S
S0
S2O32–
S2O32–
S0
H 2S
H2
H2
Fe(II)
Fe(II)
H2
NO2–
NH3
H2
Electron
acceptor
O2
SO42–
CO2
SO42–
S0
O2
O2
O2
NO3 –
NO3 –
NO3 –
O2
Fe(III)
O2
NO3 –
MnO2
O2
O2
NO3 –
Redox reaction
CH4 + 2O2 = CO2 + 2H2O
CH4 + SO42– = HCO3 – + HS – + H2O
H2 + 1/4CO2 = 1/4CH4 + 1/2H2O
H2 + 1/4SO42– + 1/2H+ = 1/4H2S + H2O
H 2 + S0 = H 2S
H2S + 2O2 = SO42– + 2H+
S0 + H2O + 31/5O2 = SO42– + 2H+
S2O3 – + 10OH– + O2 + 4H+ = 2SO42– + 7H2O
S2O3 – + 6OH– + 4/5NO3 – + 4/5H+ = 2SO42– + 17/5H2O + 2/5N2
S0 + 32/5H2O + 6/5NO3 – = SO42– + 34/5H+ + 3/5N2 + 6OH–
H2S + 36/5H2O + 16/5NO3 – = 2SO42– + 84/5H+ + 8/5N2 + 16OH–
H2 + 1/2O2 = H2O
H2 + 2Fe3+ = 2Fe2+ + 2H+
Fe2+ + 1/4O2 + H+ = Fe3+ + 1/2H2O
Fe2+ + 1/5NO3 – + 2/5H2O + 1/5H+ = 1/10N2 + Fe3+ + OH–
H2 + MnO2 + 2H+ = Mn 2+ + 2H2O
NO2– + 1/2O2 + 2OH– + 2H+ = NO3 – + 2H2O
NH3 + 3OH– + 4O2 = 3NO3 – + 2H2O
H2 + 2/5NO3 – + 2/5H2O = 1/5N2 + 8/5H+ + 2OH–
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Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Marteinsson et al., 1997; Mitsuzawa et al., 2005]. All the
investigations clearly demonstrated significantly increased
thermotolerance patterns at elevated hydrostatic pressure,
although the tolerance levels demonstrated are all within
several minutes to several tens of minutes at or below 120°C.
The gap between these laboratory experiments and observation of hyperthermophiles in situ in superheated hydrothermal fluids far above 120°C is a piece of the puzzle still to
be clarified. In addition, tolerance of and susceptibility to
metal toxicity are important physiological properties for
deep-sea vent microorganisms because gradients of potentially toxic metals are formed concomitantly with mixing
between hydrothermal fluids and ambient seawater. Vetriani
et al. [2005] hypothesize that metal toxicity for microbial
communities might be increased inversely with decreasing
concentrations of heavy metals because of the increasing
ratio of dilution by oxygenated ambient seawater, which
is associated with increased bioavailability and solubility.
This hypothesis is generally supported by experimental data
showing that thermophilic Archaea and Bacteria from higher
termperatures and more reductive habitats are more susceptible to toxic metal species, whereas mesophilic microbial
components from lower temperatures and more oxidative
habitats show higher tolerances for toxic metals [Jeanthon
and Prieur, 1990; Llanos et al., 2000; Rathgeber et al., 2002;
Edgcomb et al., 2004; Vertriani et al., 2005]. It is becoming
evident that each of these physical and chemical parameters
has a considerable impact on the growth and survival of
individual microbial components, but the potential interactive effects at the community level of physical and chemical
parameters are not well understood.
4. Back-arc basins: why they are
interesting microbiologically
4.1. Overview
Several years after the discovery of deep-sea hydrothermal
vents on MOR systems [Francheteau et al., 1979; Spiess et
al., 1980], areas of deep-sea hydrothermal venting were discovered in BABs of the western Pacific. These hydrothermal
systems, identified in Manus Basin [Both et al., 1986], Lau
Basin and North Fiji Basin [Hawkins, 1986; Hawkins and
Helu, 1986], Mariana Trough [Craig et al., 1987a, 1987b],
and Okinawa Trough [Kimura et al., 1988; Halbach et al.,
1989] (Figure 2), are geologically and tectonically distinct
from hydrothermal systems found on MORs.
From a microbiological perspective, research in BAB
hydrothermal systems has been limited. Until recently, our
understanding of microbial diversity in these environments
had been restricted to the isolation and characterization of
Figure 2. Location and tectonic setting of deep-sea hydrothermal
fields identified in arc–back-arc systems of the western Pacific
margin. Numbers indicate the hydrothermal field as follows: 1,
Iheya North; 2, Izena Hole; 3, Minami Ensei Knoll; 4, Hatoma
Knoll; 5, Yonaguni Knoll IV; 6, Myojin Knoll; 7, Suiyo Seamount;
8, Alice Spring; 9, Central Mariana Trough; 10, Off axial volcano;
11, TOTO caldera; 12, Vienna Woods; 13, PACMANUS; 14, DESMOS; 15, Station 4 (White Lady); 16, Station 14; 17, Vai Lili; 18,
Hine Hina; 19, White Church.
some novel hyperthermophilic and heterotrophic microorganisms, including Pyrococcus abysii [Erauso et al., 1993],
P. horikoshii [Gonzalez et al., 1998], Thermococcus profundus [Kobayashi et al., 1994], T. peptonophilus [Gonzalez et
al., 1995] and Thermosipho melanesiensis [Antoine et al.,
1997]. However, since the turn of this century, numerous
microbiological investigations of western Pacific BAB hydrothermal vent sites [Takai and Horikoshi, 1999, 2000; Takai et
al., 2000, 2001, 2002, 2003a, 2004a, 2004d, 2005a; Inagaki
et al., 2003, 2004; Nakagawa et al., 2004a, 2005a, 2005b,
2005c; Suzuki et al., 2004] have provided baseline culturebased and culture-independent diversity data. These data
provide a framework for comparative studies with microbial
diversity from MOR deep-sea hydrothermal systems.
In this section, we introduce the microbial communities in two different well-characterized BAB hydrothermal
systems, the PACMANUS field in the Manus Basin and the
Iheya North field in the Mid-Okinawa Trough. In addition
Takai et al.
to these two BAB hydrothermal fields, systematic and intensive microbiological explorations are under way or planned
in other BAB systems of the Southern Mariana Trough and
the Lau Basin. We discuss the significance of these BAB
hydrothermal systems and patterns of diversity revealed by
the comparison of microbial ecosystems in MOR and BAB
systems.
4.2. Case Study: PACMANUS Site in the Manus Basin
The Manus Basin, located in the Bismarck Sea, is a backarc spreading basin situated to the north of the New Britain
Island Arc-Trench system (Figure 2). The Manus Basin is
characterized by three major spreading centers (western,
central, and eastern spreading centers) linked by transform
faults. The central basin has an exceptionally high spreading
rate (>100 mm/yr [Baker et al., 1995]) and the eastern basin
is currently in a “stretching” phase [Martinez and Taylor,
1996]. Three distinct hydrothermal fields have been identified in the Manus Basin: the Vienna Woods field (Location
12 in Figure 2) in the rift valley of the central spreading basin
[Lisitsyn et al., 1993], the DESMOS caldera (Location 14 in
Figure 2) [Gamo et al., 1993, 1997], and the PACMANUS
field (Location 13 in Figure 2) in the eastern spreading
center. Based on seafloor observations and the geochemical characterization of superheated hydrothermal fluid in
the three hydrothermal fields during the DSRV Shinkai
2000 expedition in 1995, Gamo et al. [1996] described the
hydrothermal systems in the Manus Basin as follows: (1)
the Vienna Woods hydrothermal system, hosted by a basaltic lava seafloor, is comparable to MOR systems; (2) the
PACMANUS field, hosted by an andesitic lava seafloor, has
hydrothermal fluids with lower pH, lower concentrations of
Ca, and enriched with K, total inorganic carbon (TIC), and
heavy metals in comparison with MOR and Vienna Woods
hydrothermal systems; (3) the DESMOS caldera represents
a novel type of hydrothermal system, fueled by superheated
volcanic vapor and characterized by highly acidic hydrothermal fluids resulting from oxidation of volatile volcanic
sulfide gas (H2S) to sulfate.
The distribution of Archaea in a typical black smoker
chimney from the PACMANUS field was investigated [Takai
et al. 2001]. An actively venting chimney structure was
obtained from a black smoker at a depth of 1644 m (Plate 1,
A and B). The in situ temperature of the effluent hydrothermal fluid was approximately 250°C. In cross section, the
chimney was divided into four different zones (Plate 1C):
(1) an inner crystalline interface with a hydrothermal fluid
conduit, (2) a grayish porous inner layer, (3) a black solid
outer layer, and (4) a surface layer coated with orange, white,
and gray mineralized crusts [Takai et al., 2001]. Chemical
203
and mineralogical analyses revealed that the chimney consisted primarily of zinc sulfide, whereas the surface layer
was enriched with barite [Takai et al., 2001]. Based on these
characteristics, the chimney was classified as a “kuroko”type sulfide chimney, which is distinct from the copper- and
iron-rich sulfide chimneys often observed in MOR hydrothermal systems [Iizasa et al., 1999].
The distribution of Archaea in the different layers of the
chimney structure was analyzed by a variety of molecular
phylogenetic techniques, including rRNA dot-slot hybridization, quantitative fluorogenic PCR, T-restriction fragment length polymorphism, and 16S rDNA cloning and
sequencing. These analyses revealed shifts of the archaeal
community between the different layers over a distance of
several centimeters (Plate 1C) [Takai et al., 2001]. Members
of Thermococcus and the as-yet-uncultured DHVEG,
described above, were the dominant archaeal phylotypes in
the outer surface of the chimney (Plate 1C). The presence
of Thermococcales was confirmed by a semiquantitative
cultivation test [Takai et al., 2001]. Different archaeal phylotypes dominated the interior parts of the chimney [Takai
et al., 2001]. Desulfurococcales dominated the superheated
hydrothermal fluid conduit, and the major archaeal phylotype in the interior layers grouped with the extremely
halophilic Haloarcula (Plate 1C) [Takai et al., 2001]. This
was the first report of extremely halophilic Archaea in deepsea hydrothermal environments. Although no halophilic
archaeon has been isolated from deep-sea vents to date,
several halophilic Bacteria have been isolated from a range
of deep-sea hydrothermal environments. These include the
moderately halophilic Halomonas neptunia, H. sulfidaeris,
H. axialensis, and H. hydrothermalis, isolated from low-temperature hydrothermal fluids and sulfides [Kaye and Baross,
2000, 2004]; Idiomarina loihiensis [Donachie et al., 2003]
isolated from vents on the Loihi Seamount; and Clostridium
caminithermale [Brisbarre et al., 2003], first isolated from a
deep-sea vent site on the Mid-Atlantic Ridge. The formation
of hypersaline conditions in subseafloor environments of
deep-sea hydrothermal systems has been proposed to result
from phase separation and segregation of hydrothermal
fluids [Kaye and Baross, 2000]. The presence of halophilic
archaeal phylotypes and of diverse halophilic Bacteria in
deep-sea hydrothermal vent environments suggests that
hypersaline environments are present in hydrothermal subseafloor habitats.
4.3. Case Study: Okinawa Trough
The Okinawa Trough is a “rifting phase” BAB located
between the Ryukyu Arc-Trench system and the Asian continent [Letouzey and Kimura, 1986]. Since the initial discovery
204
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Plate 1. Photographs of black smoker vents of the PACMANUS field (A) and of a successfully recovered chimney
structure (B). A sketch (C) of the substructures of chimney section and the distribution pattern of Archaea corresponding to the substructures.
Plate 2. Bathymetry map of the Iheya North Knoll, including the Iheya North hydrothermal field.
Takai et al.
of submarine hydrothermal activity in the Iheya Knoll and
the Izena Hole of the Mid-Okinawa Trough (MOT) [Halbach
et al., 1989; Sakai et al., 1990; Glasby and Notsu, 2003], a
total of six active hydrothermal fields have been identified:
(1) Minani-Ensei Knoll (Location 3 in Figure 2), (2) Iheya
North (Location 1 in Figure 2), (3) Iheya Ridge, (4) Izena
Hole (Location 2 in Figure 2), (5) Hatoma Knoll (Location
4 in Figure 2), and (6) Yonaguni Knoll IV (Location 5 in
Figure 2). Several interdisciplinary investigations have been
conducted in these hydrothermal fields and have focused on
the geochemistry [Glasby and Notsu, 2003, for review] and
the microbial ecology [Takai and Horikoshi, 1999, 2000;
Takai et al., 2000, 2001, 2002, 2003a, 2004c; Inagaki et al.,
2003, 2004; Nakagawa et al., 2004a, 2005a, 2005b, 2005c;
Suzuki et al., 2004] of the hydrothermal fluids and sulfide
deposits. The vent fields of the Okinawa Trough are hosted
on felsic volcanic rocks [Ishibashi and Urabe, 1995] and
thick terrigenous sediments from the Yangtze and Yellow
Rivers [Narita et al., 1990]. Hydrothermal fluids in the
Okinawa Trough vent fields are characterized by high concentrations of gaseous carbon compounds [Ishibashi et al.,
1990; U. Tsunogai et al., unpublished data, 2002], which
are highly depleted in 13C-CH4 and moderately depleted in
13C-CO [U. Tsunogai et al., unpublished data, 2002], and
2
phase separation appears to be controlling the chemistry
[Kataoka et al., 2000]. Liquid CO2 and CO2 hydrates are
distributed in the sediments of the vent fields [Sakai et al.,
1990]. Thus, the geological, physical, and chemical features of the Okinawa Trough vent fields are characteristic of
sediment-hosted, back-arc rifting systems along continental
margins and are distinct from spreading centers in MOR
hydrothermal systems.
The Iheya North vent field is the best characterized vent
field in the Okinawa Trough. The Iheya North field is located
on the northwest edge of the central depression of the Iheya
North Knoll (Plate 2). Six large hydrothermal mounds,
named the North Edge Chimney (NEC), Event 18 (E18),
North Big Chimney (NBC), Central Big Chimney (CBC),
High Radioactivity Vent (HRV), and South Big Chimney
(SBC), are currently recognized in this field (Plate 3). The
205
highest fluid temperatures (311°C) and the highest flow
rates have consistently been recorded at the NBC mound,
suggesting that the NBC is situated over the main conduit
of hydrothermal flow. All of the mounds (except HRV) are
aligned north to south with the NBC at the center (Plate 3).
Fluid temperatures and flow rates systematically decrease
away from the NBC. In addition, the hydrothermal fluid
chemistry is significantly different between the different
hydrothermal mounds (Table 5). The composition of the
NBC hydrothermal fluids has been relatively stable during
the last 5 years, with chlorinities ranging between 75% and
100% of seawater chlorinitiy (Table 5). This range suggests
that the hydrothermal fluids from NBC have experienced
moderate phase separation and that the mixing ratio of vapor
and brine phases is stable. In contrast, the CBC hydrothermal fluids appear to be brine-rich, and the SBC and E18
hydrothermal fluids, which exhibit lower chlorinities, may
be strongly influenced by vapor-phase input (Table 5). These
variations in fluid compositions strongly suggest the occurrence of phase separation and the remixing of the vapor and
brine phases at different ratios. The mixing ratios probably
depend on the local subseafloor hydrogeologic structure.
The large physical and chemical differences between the
various hydrothermal mounds in the Iheya North vent field
could generate numerous discrete microbial habitats that
could act as a natural labratory for comparing differences in
the microbial diversity and community structure. Research
on the microbial diversity of the Iheya North field has been
conducted with an emphasis on understanding the distribution of thermophilic microorganisms present in superheated
hydrothermal fluid and in sulfide chimneys from different
hydrothermal mounds and characterized by physical and
chemical heterogeneity [Takai et al. 2003a, 2004b; Nakagawa
et al., 2005a]. Culture-independent molecular phylogenetic
analyses were used to characterize the microbial communities in near-end-member hydrothermal fluids of the NBC
(311°C), the chimney conduit walls, and ISCS deployed in
the chimney conduits [Takai et al., 2003a]. The microbial
diversity among the different samples was very similar and
consisted of bacterial and archaeal phylotypes that grouped
Table 5. End-member chemical compositions of the hydrothermal fluids obtained from various hydrothermal mounds in the Iheya
North field.
Hydrothermal
fluid from
Maximum
temp. (°C)
311
205
247
70
4
Year
1997
2000
1998
1997
Mg
mM/kg
NBC
0
SBC
0
CBC
0
E18
0
Seawater
52.7
Data from Kataoka et al. [2000] and Nakagawa et al. [2005a].
Ca
mM/kg
Na
mM/kg
K
mM/kg
Sr
μM/kg
Cl
mM/kg
18.1
2
19.9
11.9
10.2
405
8
745
288
463
73
11.8
79
56.2
9.8
65.9
13.3
67.4
53.4
87
511
24
864
338
540
Plate 3. Microbial communities at three different hydrothermal mounds in the Iheya North field. The maximum temperatures of each hydrothermal
vent fluid are shown in parentheses in the map. Columns indicate the culturable cell population of each phylogenetic group as determined by serial
dilution culture and subsequent phylogenetic analysis. The total cell counts were determined by direct cell counting of DAPI-stained cells. Stack
columns indicate the composition of microbial population based on taxonomic grouping of 16S rRNA gene clone sequencing. The ratio of Bacteria/
Archaea of the total microbial community was determined by using real-time PCR.
206
Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Takai et al.
with mesophilic ε-Proteobacteria and the as-yet-uncultured
Crenarcheota MGI, respectively [Takai and Horikoshi, 1999;
Nakagawa et al., 2005a]. As discussed, ε-Proteobacteria are
typically identified in a wide range of deep-sea hydrothemal
vent environments, whereas MGI are the most abundant and
widely distributed Archaea in the global ocean biosphere.
Both phylotypes are characteristically found in the mixing
zone between hydrothermal fluid and seawater [Takai et al.,
2004b].
Cultivation-based analyses of the ISCS deployed in hydrothermal chimney conduits detected hyperthermophilic
Thermococcocales, which suggests the presence of an indigenous microbial community in the superheated hydrothermal
fluid of NBC [Nakagawa et al., 2005a]. Furthermore, thermophilic Archaea, such as Thermococcales, Archaeoglobales,
and Methanococcales, and thermophilic and mesophilic
Bacteria, including the Aquificales and ε-Proteobacteria,
were frequently cultured from different layers of the NBC
chimney (Plate 3) [Nakagawa et al., 2004b].
Higher density microbial communities were detected in
the ISCS deployed in the brine-rich CBC vent fluids (Plate
3) [Nakagawa et al., 2005a], suggesting that differences
in population density between the NBS and CBC mounds
may result from differences in the physical and chemical
properties between the two vents. The CBC mound, with
its brine-rich hydrothermal fluids, may provide more spatially abundant and diverse subseafloor microbial habitats
than does the NBC mound. In contrast, the microbial diversity of the E18 vapor-rich hydrothermal fluids was distinct
from the microbial diversity in both the NBC and CBC
mounds (Plate 3) [Nakagawa et al., 2005a]. The microbial
community discovered in the ISCS deployed in the lower
temperature (70°C) hydrothermal fluids of the E18 mound
was mainly composed of thermophilic methanogens closely
related to Methanothermococcus okinawensis [Takai et al.,
2002; Nakagawa et al., 2005a]. E18 hydrothermal fluids are
characterized by a vapor phase and are comparable with
hydrothermal fluids from the SBC mound (Table 5), which
are enriched in CO2 and CH4 [U. Tsunogai et al., unpublished
data, 2002]. The SBC chemistry suggests that E18 fluids are
similarly enriched. High concentrations of CO2, CH4, and
perhaps H 2 in the hydrothermal fluids correlate with the
presence of thermophilic methanogens in the ISCS deployed
on the E18 mound.
The results from these analyses of microbial diversity
and community structure provide compelling evidence for
significant intrafield heterogeneity of the indigenous microbial community, which may correlate with the substantial
differences in the physical and chemical properties of the
high-temperature habitats of the Iheya North deep-sea hydrothermal field. The question of correlation points to the need
207
for further research to improve our understanding of factors
that control the distribution of microorganisms in BAB deepsea hydrothermal vent environments.
To understand how the microbial diversity of deep-seavent thermophilic environments differs from the microbial
diversity of planktonic communities in the surrounding
seawater, Takai et al. [2004b] used culture-independent
molecular phylogenetic techniques to characterize the microbial diversity in planktonic habitats near several of the Iheya
North hydrothermal mounds. Notably, the MGI phylotypes
were identified in every environment investigated, including
near-end-member fluids. Further, the abundance of MGI in
the microbial community appeared higher in the ambient
seawaters around hydrothermal plumes than in ambient deep
seawater of the Mid-Okinawa Trough [Takai et al., 2004b].
These results support the hypothesis of Moyer et al. [1998]
that deep-sea hydrothermal systems are potential sources or
sinks of the uncultivated MGI [DeLong, 1992; Fuhrman et
al., 1992].
The distribution of ε-proteobacterial phylotypes was considerably different from that of the MGI. ε-Proteobacteria
were significantly more abundant in the hydrothermal
plumes than in the seawater surrounding the plumes and
were only a minor component in the ambient deep seawater
planktonic community of the Mid-Okinawa Trough [Takai
et al., 2004b]. The dominance of ε-Proteobacteria in the
hydrothermal plumes is supported by quantitative cultivation analysis [S. Nakagawa et al., unpublished data, 2005d].
Similar distribution patterns of the MGI and ε-Proteobacteria
were also found in the Kairei field of the Central Indian
Ridge [Takai et al., 2004b], suggesting a typical distribution
pattern of the planktonic microbial communities in global
deep-sea hydrothermal systems.
Recently, more than 150 strains of thermophiles or chemolithoautotrophic mesophiles have been isolated from the Iheya
North field [Takai and Horikoshi, 2000; Takai et al., 2002,
2003a; Inagaki et al., 2003, 2004; Nakagawa et al., 2005a,
2005b, 2005c]. Several of the isolates represent new genera
or species. Thermosipho japonicus is an extremely thermophilic, fermentative bacterium [Takai and Horikoshi, 2000]
isolated from the NBC chimney. Another member from the
Thermotogales, Thermosipho melanesiensis, was isolated from
the Lau Basin [Antoine et al., 1997]. From the NBC chimney,
Methanothermococcus okinawensis is the first thermophilic
methane-producing archaeon isolated from a deep-sea hydrothermal system in the western Pacific margin [Takai et al.,
2002]. This archaeon is physiologically similar to M. thermolithotrophicus [Huber et al., 1982] but is phylogenetically associated with the mesophilic Methanococcales: Methanococcus
aeolicus [Schmid et al., 1984]. In addition, many of the previously uncultivated ε-Proteobacteria have been isolated from the
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Microbial Ecology of Mid-Ocean Ridges and Back-Arc Basins
Okinawa Trough deep-sea hydrothermal systems, including
the Iheya North field [Inagaki et al., 2003, 2004; Takai et al.,
2003a; Nakagawa et al., 2005a, 2005b, 2005c]. These isolates
include phylotypes related to all of the family-level phylogenetic
subgroups, many of which had no representatives in culture
[Takai et al., 2003a]. For example, Sulfurimonas autotrophica
[Inagaki et al., 2003] within Group B; Sulfurovum lithotrophicum [Inagaki et al., 2004] and Nitratifractor salsuginis
[Nakagawa et al., 2005c] within Group F; and Thioreductor
micantisoli [Nakagawa et al., 2005b] within Group G have been
described as new genera. Many thermophilic strains phylogenetically associated with the genera Hydrogenimonas [Takai et
al., 2004d] or Nitratifractor [Nakagawa et al., 2005c] within
Group A or the genus Lebetimonas [Takai et al., 2005a] within
the order Nautiliales (Group D) [Miroshnichenko et al., 2004]
have also been isolated from the Okinawa Trough hydrothermal
systems [Nakagawa et al., 2005a].
4.4. Other BAB Systems
The microbial ecosystems of the deep-sea hydrothermal fields in the Okinawa Trough are exceptionally well
characterized with respect to other BAB and MOR hydrothermal systems. However, the Okinawa Trough is not a
typical example of BABs along the western Pacific margin.
The Mariana Trough and the Lau Basin are the dominant,
active intra-oceanic BABs and exhibit various phases of segments from early rifting to mature spreading [Fryer, 1995;
Hawkins, 1995].
Several microbiological research projects in the Mariana
Trough are now under way. The TOTO caldera is a submarine volcano located in the southernmost Mariana Trough
(Figure 2, Location 11). Active hydrothermal venting in the
depression of the TOTO caldera was discovered in 2000
with the ROV Kaiko [Gamo et al., 2004], and in 2003 the
geomicrobiology of the TOTO caldera hydrothermal field
was investigated by using the DSV Shinkai 6500. As a result
of this latter expedition, several novel chemolithoautotrophs
were isolated and characterized [Takai et al., 2004e, 2005a],
and the microbial communities of the hydrothermal fluids
and chimney structures were described using both culturebased and culture-independant techniques [Nakagawa et
al., 2006]. Approximately 20 km northeast of the TOTO
caldera, a new deep-sea hydrothermal field hosting vigorous black-smoker activity was discovered in 2003 (Figure 2,
Location 10). This deep-sea hydrothermal system is located
on the off-axis volcanoes in the Mariana Trough and is
comparable to hydrothermal systems recently discovered on
a number of other submarine volcanoes along the volcanic
front of the Mariana Arc [Embley et al., 2004] and to two
previously reported axial hydrothermal fields in the central
Marina Trough (Figure 2, Locations 8 and 9) [Craig et al.,
1987b; Hawkins et al., 1990]. In the southern Lau Basin,
three active hydrothermal fields, named Vai Lili (Figure 2,
Location 17), Hine Hina (Figure 2, Location 18), and White
Church (Figure 2, Location 19), were identified along the
Valu Fa Ridge [Fouquet et al., 1990, 1991a, 1991b, 1993].
The Vai Lili field is well-known for the unique chemistry of
its hydrothermal fluids, which are characterized by very low
pH and highly enriched in dissolved base metals (Zn, Pb, Cu,
and Cd) [Herzig et al., 1993]. Most likely, the unique chemistry of the hydrothermal fluids will support novel microbial
communities and geobiological interactions. Nevertheless,
except for numerical taxonomy of heterotrophs by Durand
et al. [1994], the isolation of T. melanesiensis [Antoine et
al., 1997], and the research on heavy metal toxicity on Lau
microbes, very little work has been done to understand the
community structure and dynamics in the hydrothermal
fields of the Lau Basin. Ongoing and future microbiological
investigations in the Mariana Trough and the Lau Basin will,
no doubt, reveal microbial diversity patterns different from
those observed in the Manus Basin and Okinawa Trough and
will provide a more thorough understanding of the microbial
ecology of the dominant, active intra-oceanic BABs of the
western Pacific. Further, these studies may provide important information about the biogeography of microorganisms
in deep-sea hydrothermal systems globally.
5. Concluding remarks
Much of our understanding of the microbial ecology of
deep-sea hydrothermal vents stems from research focused on
MOR systems. However, recent research on the microbiology
of BAB) and VA hydrothermal vents reveals a greater heterogeneity of microbial communities between vent systems than
previously thought. Furthermore, this heterogeneity can be
directly correlated to differences in the physical and chemical properties between different vent fields. By comparing
MOR, BAB, and VA systems, microbiologists can begin to
develop an overview of the patterns of microbial diversity
in deep-sea hydrothermal systems globally. As described
in this review, culture-independent methods are now routinely being used in microbial ecology together with more
traditional culture-dependent methods. These techniques
will enable much more reliable interfield comparisons of
microbial diversity among the MOR, BAB, and VA hydrothermal fields. Concurrently, microbiological investigations
combined with developing technology for in situ physical and
chemical measurements could link the emerging diversity
and ecophysiological functions of microbial communities to
the physical and geochemical variations in deep-sea hydrothermal vent environments.
Takai et al.
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