Review
The future of coral reefs: a microbial
perspective
Tracy D. Ainsworth1, Rebecca Vega Thurber2 and Ruth D. Gates3
1
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4810, Australia
Florida International University, Department of Biological Sciences, Biscayne Bay Campus, North Miami, FL 33181, USA
3
Hawaii Institute for Marine Biology, SOEST, University of Hawaii, HI 96744, USA
2
Microbial communities respond and quickly adapt to
disturbance and have central roles in ecosystem function. Yet, the many roles of coral-associated microbial
communities are not currently accounted for in predicting future responses of reef ecosystems. Here, we propose that a clearer understanding of coral-associated
microbial diversity and its interaction with both host
and environment will identify important linkages
occurring between the microbial communities and
macroecological change. Characterizing these links is
fundamental to understanding coral reef resilience and
will improve our capacity to predict ecological change.
Microbial communities and the future of coral reefs
The future state of coral reefs will be determined by the
ability of the ecosystem to respond to increasing environmental disturbances while remaining a coral dominated
system [1,2]. Complex microbial communities are known
to be extremely important members of many ecosystems [3–
5], and also has significant influence over coral reef ecosystems. In terrestrial ecosystems, microbes have pivotal roles
in, and sustain important linkages between, aboveground
and belowground processes [6]. In these ecosystems, the
microbial community is extremely sensitive to environmental change, and following disturbance, these communities
remain altered and functionally different for long periods of
time. It is believed that these microbial community
dynamics are as important as plant communities in predictive modeling of ecosystem change [7]. In coral reef
ecosystems the ways in which microbial communities function are likely to be as complex, diverse and as important to
whole ecosystem function as those of other ecosystems.
The coral reef provides a structurally and environmentally complex array of habitats, which support a broad
microbial diversity that influences both host physiology
and ultimately ecosystem processes. Microbial processes
and metabolisms strongly influence biogeochemical and
ecological processes within the reef environment, such as
food webs, organism life cycles, and chemical and nutrient
cycling; all of which are fundamental to ecosystem
stability. Microbial processes are also key drivers of the
many factors that influence the resilience of coral reef
ecosystems, such as larval recruitment, colonization, and
overall species diversity. For example, chemical cues from
the benthic microbial communities influence the settlement of larvae of many keystone species, including corals
and sea urchins [8,9]. Also, endosymbiosis between corals
and the eukaryotic dinoflagellate genus Symbiodinium is
responsible for the evolutionary success of stony corals in
the shallow tropics and the long-term survival of the coral
reef ecosystem [10,11]. Given their established roles in
ecosystem functioning, it is surprising how little research
has been aimed at understanding the linkages between the
broader microbial ecology (communities of bacteria,
Achaea, viruses and fungi) and macroecological shifts on
reefs. Only recently have the role of microbial diversity and
host–microbe interactions in the response of reef ecosystems to environmental change been explored.
Although we recognize that complex microbial interactions probably exist for all reef organisms, here we focus
specifically on the microbial interactions with stony corals
as a rationale for incorporating microbial ecology into
future studies investigating coral reef resilience. We argue
that by incorporating microbial ecology into studies of coral
reef ecological change, we will improve our capacity to
predict and model the consequences of environmental
disturbances on coral reefs.
Glossary
Biofilm: an aggregation or community of microbes growing on an
environmental surface (for examples see [8,71]).
Coral Holobiont: the holobiont is the collective community of coral
host and its metazoan, protist, and microbial symbionts (see [11]).
Coral microbiome: the collective genome of the coral-associated
(symbiotic and non-symbiotic) micro-organisms.
Keystone species: a species that is crucial to the structure of the
ecosystem.
Koch’s postulates: a system to determine causation of disease by a
specific microbe (etiological agent).
Microbiome: the collective genome of microorganisms or microbial
assemblage (Bacteria, Archaea, and protists) associated with any
system such as the body of an animal, a water or soil sample, or an
entire ocean.
Microbial community: an assemblage or population of microbes
Metagenomics: the study of nucleic acids from a given source,
including environmental samples. The technique is usually applied
to determine both the composition (diversity) and capabilities (function) of a community of organisms (for review [72]).
Next generation sequencing: rapid high-throughput sequencing of
large sample sets (for reviews [73,74]).
Resilience: the capacity of an ecosystem to absorb disturbance (for
reviews see [1,75,76]).
Scleractinia: the order Scleractinina (within the Anthozoans) are the
stony or hard corals.
Symbiosis: a close interaction or association between evolutionarily
distinct organisms (for review of marine invertebrate symbiosis see
[10]).
Corresponding author: Ainsworth, T.D. ([email protected]).
0169-5347/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2009.11.001 Available online 16 December 2009
233
Review
Identification of the coral holobiont and the coral reef
microbiome
During the 1990s, it became increasingly apparent that
marine microbial diversity was orders of magnitude higher
than previously believed. Fuhrman and Campbell [12] indicated that upwards of 95% of marine bacterioplankton could
not be cultured. Following this, Rohwer and colleagues [11]
successfully applied culture-independent techniques to
describe the microbial communities associated with the
Caribbean coral Montastraea franksi. Using variations in
the third hypervariable region (V3) and sequencing of the
16S rRNA gene, it was found that approximately 30% of
coral-associated bacterial phylotypes were similar to Cyanobacteria and a-Proteobacteria species. By contrast, the
cultivable bacteria were found to be dominated by the
Pseudoalteromonads and Vibrio spp. and members of the
Cytophaga–Flavobacter Flexibacter–Bacteriodes group
(CFBs). This study revealed that the diversity of bacteria
on corals was significantly greater than previously believed
and demonstrated that culturing methods do not accurately
reflect the composition or diversity of the microbial populations living on coral reefs. Coral-associated microbial
communities have subsequently been shown to be highly
diverse >50% of the ribotypes were less than 63% similar to
those in the database [11]. Individual coral species have a
unique and stable microbial fingerprint that is distinct from
the water column [13,14]. However, microbial diversity [15]
and specific coral–microbe associations [16] have also been
shown to vary between reef locations and also along the
length of coral host branches [13]. The specificity of coral–
microbial associations is evidently more complex than current estimates predict and is probably strongly influenced
by host and environmental variability.
Coral-specific microbial communities are hypothesized
to have important physiological and ecological roles on
coral reefs. For example, microbial-mediated nitrogen fixation on corals was first proposed in 1987 [17]. It has since
been demonstrated that some coral species contain intracellular bacteria that are capable of nitrogen fixation [18].
This occurs during periods when host intracellular oxygen
concentrations are low; conditions which are driven by the
endosymbiotic eukaryotic dinoflagellate photosynthesis
[18,19]. Other reports have found that coral-associated
Archaea conduct ammonium oxidization and nitrogenous
waste removal for the coral host [20]. The coral microbiota
is further believed to provide a protective role for their
coral hosts through the production of antibiotics and the
occupation of physical space and competition with invading
or opportunistic pathogens [21]. This overall model that
corals exist in a multipartite symbiosis with both endosymbiotic dinoflagellate and resident microbiota (bacteria
and Archaea) has been termed the coral holobiont
[11,17,18,20,21]. Yet, the current opinion that members
of the coral-associated microbial communities have both
beneficial and negative roles in coral and reef ecosystem
function are in fact supported by little direct evidence.
This is because of limitations in both the technological
approaches to document microbial community composition
and the overall complexity of the coral reef microbiome.
Initially the field of coral reef microbiology was dominated by culture based identification of bacterial pathogens
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Trends in Ecology and Evolution Vol.25 No.4
[22–25] and specifically the application of Koch’s postulates
[22–25]. Although these studies raised awareness of the
potential importance of microbes on reefs, these approaches
did not address the complexity of the coral–microbial communities or the nature of host–microbe interactions. The
identification of single etiological agents associated with
patterns of coral mortality is constrained by several important microbial and coral phenomena. The vast majority of
marine microbes require complex nutritional and/or
physical conditions that have yet to be replicated in culture
conditions. In addition, microbes often exist in interdependent assemblages functioning as single metabolic units,
scenarios that cannot be replicated in monoculture conditions. Also, microbes often exist in highly specific relationships with their hosts, and the absence of key host factors
inhibits culture. Furthermore, the signs of coral disease are
inherently vague [26,27] and degraded coral tissues are
rapidly colonized within the marine environment, significantly altering both the microbial community and its interaction with the host. By not acknowledging these limitations
in the application of culture based studies to coral microbial
ecology, we limit our understanding of the complex role of
coral microbial communities in reef stability, their
responses to climate change, and their role in coral reef
responses. Finally, studies of microbial diversity have relied
on phylogenetic markers to infer the metabolic potential of
the community. However, microbes with almost identical
ssrRNA genes can have vastly different physiology, and
subsequently, have very different roles in ecosystem function (Box 1). These factors need to be considered in investigations of the significance and roles of microbial
communities in ecological change on coral reefs.
Many recent studies are now providing compelling evidence that coral–microbial associations are more complex
Box 1. Overcoming the limitations of phylogenetic markers
to characterize microbial community function.
Phylogenetic markers, such as the small subunit of the ribosome,
are useful for characterizing the diversity of the microbial community but reveal little about the metabolic capabilities of organisms.
Physiological differences among phylogenetically related taxa can
occur owing to gene duplications, insertions and deletions, as well
as through horizontal gene transfer events such as plasmid
acquisition or the incorporation of viral genes. An example of this
phenomenon is the cyanobacteria Prochlorococcus. Strains of this
bacteria are found in almost all tropical oligotrophic habitats, but
vary in abundance with latitude and depth [77]. These strains have
almost identical 16S sequences (97% similarity), but differ
physiologically [78]. Termed ecotypes, each Prochlorococcus strain
is spectrally tuned to reside within a given light regime [79]. High
light-adapted Prochlorococcus are abundant at the sea surface and
have remarkably small genomes encoding only 1700 proteins. Low
light-adapted Prochlorococcus are abundant at depths of 200 m and
have larger genomes that encode for 2300 genes [78]. Similar
variations in genome size can be found in Vibrio splendidus where
70% of the 206 strains that make up a single Vibrio splendidus
ribotype cluster have differences in genome size even though the
16S genes of these strains are < 1% divergent [80]. In this case, the
size variations range from 4.5 kb to 5.6 kb and are not driven by the
presence of bacterial plasmids [80]. Perhaps more importantly, it
has been shown that the presence of a single gene variant can alter
both the microbial host range and the interactive status of a
microbial symbiosis from benign or beneficial to pathogenic [81].
Metagenomics enables the functional capacity of microbial communities to be characterized in an ecologically relevant setting.
Review
than previously estimated and are significantly influenced
by factors specific to both the physical [15,16] and the host
environment [13,18,18,18,28]. Only by addressing the true
complexity of the microbial habitat and the strong influence of environmental and host factors can we understand
the role of microbial communities in coral reefs ecosystems
and incorporate these communities into predictive models
of future ecosystem stability.
Habitat complexity and microbial diversity
Coral reefs are formed as a result of calcium carbonate
deposition by scleractinian corals, and these vast biological
structures form complex habitats for an enormous diversity of marine life (Figure 1), including microbial communities. Factors, such as temperature, light and water flow,
vary significantly over these complex structures and influence both the host and the microbial communities [29–31].
The scleractinian coral hosts exhibit highly plastic
morphologies (both within and among coral colonies) in
response to the environment, modifying the microbial
environment [32–36]. Therefore, just as the reef provides
a multitude of niches for macro-organisms, each coral
colony contains numerous microhabitats for an array of
microbial communities (Figure 2, Box 2).
Microhabitats found on and within coral structures
support diverse microbial communities and influence
microbial function within the coral holobiont. For example,
in branching corals, branch tips are exposed to higher light
intensities and more rapid water flow than are the bases of
the branch. These differences result in rapid host tissue
growth and low endosymbiotic dinoflagellate (Symbiodinium spp.) densities at the tip, and comparatively slow
host tissue growth and high endosymbiotic dinoflagellate
densities at the base of the branch [37]. The variability in
endosymbiont density occurs on extremely small scales
within the coral colony [38,39], strongly influences host
growth and calcification [40], and the surface environment
[27,28]. Fang and colleagues demonstrated a metabolic
Figure 1. The complex coral reef structure. The coral reef environment is a
structurally complex system with extensive species (both within and between
genera) and habitat diversity that supports an array of microbial life.
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diffusion gradient from the base of a coral branch (dense
endosymbionts) to the rapidly growing tip (without endosymbionts), which facilitates rapid metabolism, growth
and calcification in the host [40]. Kuhl et al. [39] showed
that coral tissue surface O2 saturation fluctuates daily
from >250% air saturation following light exposure to
<2% air saturation following dark exposure, and that
pH of the coral surface rapidly varies from 8.5 (during
light conditions) to 7.3 (during dark conditions). Furthermore, Ulstrup et al. [38] demonstrate that oxygen saturation of the tissue surface varies significantly between the
coral polyp and connective tissue between polyps (cenosarc), and that variability in oxygen saturation is further
influenced by light availability of the environment (e.g. in
bright and shaded areas) on the reef. These differences in
microhabitats within the coral colony and within the reef
environment will also impact members of the microbial
community. Comparisons of the microbes from the coral
surface mucus layer (or surface biofilm), the intracellular
spaces within host tissues, and the skeletal matrix show
that each community is distinct. Rohwer et al. [13] demonstrated that the diversity of bacterial communities associated with coral varied across the length of the coral branch.
The internal environment of the coral host is also impacted
by abiotic parameters, such as light penetration to the
skeleton, and these factors have been shown to influence
the endosymbiotic dinoflagellate populations [41] and also
the endolithic microbial communities within the coral
skeleton [42,43]. However, the means by which the extent
of microenvironment variability and the resultant coral
microbial ecology is ultimately manifested in the physiology and performance of the coral reef is yet to be explored.
In other systems, microenvironmental variability significantly impacts both the host organism’s physiology and
ecosystem function. For example, biofilms and microbial
associations of plant surfaces are strongly adapted to, and
influenced by, small-scale environmental variability. Factors such as surface chemistry, nutrient availability, and
water saturation, which are specific to plant microhabitats,
such as leaf surfaces, stems and shoots, influence the
microbial associations within each habitat [44]. Patchy
or non-uniform environmental factors further influence
plant root growth and formation, and, in turn, also influence the composition of microbial communities of both the
root nodules and the surrounding soil [45].
Corals similarly create complex and heterogeneous
microhabitats for microbial life, and the microbial diversity
of these habitats is potentially as significant to host physiology as it is in other systems. Microhabitat partitioning
strongly influences the composition of microbial communities, the contribution of the microbial community to host
physiology (as a multipartite symbiotic entity or holobiont), and the role of the host within the ecosystem
[11]. The idea that the coral holobiont, or any other organism in the reef ecosystem, represents a stable and uniform
habitat vastly over-simplifies these complex and dynamic
systems, and is likely to lead to misinterpretations of
experimental data and the role of microbes in coral stress,
bleaching and disease [46–48]. Understanding microbial
diversity and the interaction of this diversity within a
highly complex and variable host environment is essential
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Trends in Ecology and Evolution Vol.25 No.4
Figure 2. The complexity of the coral reef structure results in many microhabitats. The host structure provides various microhabitats for microbial colonization within the
coral colony, coral polyps and coral tissues. Each microbial compartment on the reef is influenced by physical and biological environmental conditions that vary in time and
space. Environmental variability through the water column (dark blue arrow) is related to reef depth and reefal position. Biological variability along the branch axis (brown
arrow) is related to environmental (light and water flow) and biological factors (colony openness, endosymbiotic dinoflagellate density, respiration and photosynthesis).
Variability along the branch apical to the basel axes (green arrow) is related to the variable 3-dimension structure of host, polvp density, and niche environments for
microbial colonization and biofilm formation.
to understanding the role of microbial communities in coral
responses to environmental change.
Environmental influences on the coral microbiome
Environmental changes to reef ecosystems are now considered an unavoidable feature of coral reefs [49]. These
worldwide declines in tropical reefs are linked to a variety
of environmental problems, many of which are predicted to
increase in severity in the future [2,50]. The impact of these
problems, particularly thermal stress (which results in
mass coral bleaching), on the physiology of corals and their
eukaryotic microbial endosymbionts (Symbiodinium spp.)
has been widely investigated in recent years (reviewed in
[51]). However, the physiological changes occurring within
the coral host in response to environmental stressors will
also alter other host–microbe interactions. The effects of
environmental stress on the host and its associated
236
microbial communities include: loss of mucus from the
coral surface, reduced mucus supply to the coral surface
mucus layer, changes in nutrient availability, impaired
endosymbiotic dinoflagellate function, and also host tissue
breakdown [52–56]. Environmental stressors that impact
host physiology also change the microbial environment and
subsequently the microbiome. Bourne et al. 2007 demonstrated that changes in microbial communities are evident
in bleached coral colonies when compared to healthy coral
in the months before bleaching and in coral following
recovery [49]. The authors are rightly cautious in attributing pathogenicity to specific microbial changes, as environmental changes will impact the coral holobiont in a
multitude of ways.
Microbial metabolism and physiology are directly
affected by the same environmental disturbances that
alter host metabolism, and these changes will alter the
Review
Box 2. Host partitioning of the microhabitat
Typically, hundreds to thousands of individual polyps form a single
coral colony and form niche environments in which microbial
communities can establish and impact the host physiology. Regions
such as the coral tentacles, mouth and gut harbor microbial
communities as a result of feeding, and host-specific interactions
occur within the surface mucus layer and within the coral tissues
and exposed coral skeleton. Similar to surface microbial communities in other systems, the coral surface mucus layer forms a
microbial biofilm which is strongly influenced by the coral and the
photosynthetic endosymbiotic dinoflagellates (Symbiodinium spp.)
The host environment and surrounding seawater provide and
sustains nourishment to the mucus layer (reviewed in reference
[56]) and its associated microbial communities [21].
However, intracellular microbial symbionts other than the endosymbiotic dinoflagellates (Symbiodinium spp.) are rarely observed in situ. Some bacterial endosymbioses of coral host tissues
have been proposed to occur within the coral gastroderm (or
endoderm) a tissue layer that also houses the endosymbiotic
dinoflagellates [19,25,27,82]. In addition, Lesser et al. [18,28] have
also provided evidence for endosymbiotic cyanobacteria in epithelial tissues of some, but not all, color morphs of Montastrea
cavernosa in the Caribbean. The calcium carbonate skeletal matrix
of reef-forming corals harbors diverse microbial communities,
supporting photosynthetic algae and cyanobacteria within the
endolithic layer, which is visible as a green layer below the coral
tissues in many massive coral species. Other members of the
endolithic microfauna include microalgae, fungi, cyanobacteria and
bacteria.
interaction between the coral host and the microbial community within each microhabitat. Although this has not
yet been studied in corals, the impacts of environmental
changes on ecosystem function via direct and indirect
effects on the microbial communities have been documented in other systems. For example, soil plant–microbe
interactions are considered important drivers of plant
community ecology [57] and these are influenced by
environmental change. The community of ammonia-oxidizing bacteria within grasslands responds to environmental
changes such as increased atmospheric CO2, temperature
and precipitation. These feedback onto the ecosystem by
significantly altering nutrient cycling [58]. Invasive plant
species alter the soil microbial community structure and
function and, ultimately, the soil environment, compared
with native species [59,60]. Interestingly, recent work by
Stat and Gates [61,62] report one endosymbiotic dinoflagellate clade (subspecies) is an invasive (non-native) symbiont of corals on Hawaiian reefs and is linked to increased
host susceptibility to disease and mortality. In such
examples, both direct and indirect effects of environmental
change and stress on microbial community structure and
function result in consequences that are evident within the
ecosystem. Documenting the complexity of microbial community and holobiont responses to environmental stress,
and their subsequent role in macroecological change, is
therefore fundamental for predicting reef change.
Documenting the responses of the coral reef
microbiome
Metagenomic approaches overcome the limitations of
previous diversity and culture-based studies and provide
a means to assess the complex roles that microbes
play in virtually any ecosystem. This approach allows
Trends in Ecology and Evolution
Vol.25 No.4
simultaneous assessment of coral-associated microbial
diversity, microhabitat and functional responses of the
microbiome. Metagenomics uses high throughput sequencing to characterize entire microbial assemblages or
metagenomes within a given system using phylogenetic
markers (e.g. ssRNA, RecA, DNA polymerase) to provide
insight into the diversity of the community in combination
with the identification of protein encoding gene sequences
to identify the potential metabolic pathways available
within the community. This technology has been applied
to microbial and viral consortia from a variety of environments, experimental scenarios [63–66] and temporal and
spatial scales (Figure 3) [67]. Studies using metagenomics
methods have also begun to unveil the functional roles of
unique microbial communities [67]. Wegley et al. [20],
found that coral microbial communities significantly contribute to coral holobiont protein and nitrogen cycling.
Another recent metagenomic study has found that significant shifts in the functional capacity of the coral-associated
microbiome occur when the coral is exposed to abiotic
stress [68]. A microbial community (all organisms less
than 8 mm) present on Pacific corals exposed to thermal,
pH, nutrient, and carbon stress shifted from a community
with few virulence genes to one with an abundance of genes
involved in pathogenesis. Therefore, this study hypothesized that small, albeit significant, metabolic changes are
much more important than changes in the structure of a
microbial community when determining the ability of a
system to adapt to local environmental shifts. Such a
hypothesis could be extrapolated to whole ecosystems.
For example, Dinsdale et al. [69] examined the microbial
communities (<0.45 mm) from waters adjacent to four
central Pacific islands. They found significant differences
in both the abundance and metabolic capacity of the
microbial populations with location [69]. Although the
islands were different oceanographically, the dramatic
difference in microbial metabolic function indicated that
proximity to human populations and local disturbance
significantly influenced microbial diversity and metabolism and as a result influenced coral reef health.
The information acquired using these large-scale
sequencing approaches provides compelling evidence that
microbial communities are highly complex, environmentally and temporally dynamic, and extremely significant in
terms of host animal physiology and ecosystem function.
These results are provocative and provide ample rationale
for incorporating metagenomic analyses and a microbial
community perspective into studies and predictive models
of ecological change on not just coral reef systems, but all
ecosystems. We acknowledge that these approaches currently have limitations, including high costs and requirements for additional computational infrastructure. Rapid
advances in technology are already reducing cost and
bioinformatic tools for the analysis of metagenomic are
improving very rapidly.
Future directions
In considering the future sustainability of coral reefs
worldwide, it is fundamental to evaluate and understand
the complex roles that microbial communities have in
the processes that govern ecological change in these
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Trends in Ecology and Evolution Vol.25 No.4
Figure 3. The application of metagenomics to coral microbial ecology. The application of metagenomics to the coral microbiome allows scientists to explore microbial
diversity and the reef system metabolic capacity simultaneously.
ecosystems. Whereas a range of hypotheses related to the
role of microbial communities on coral reefs have been
presented in the literature, few have been tested. To begin
to address this gap, we pose a series of questions that once
addressed, will provide insight into the roles of microbes
and host–microbe interactions in large-scale ecosystem
processes on coral reefs.
1. When are coral–microbial partnerships established and
how are they maintained throughout host life cycles?
2. In what ways do environmental changes influence the
host–microbe interactions?
3. Are specific host–microbe associations indicative of
coral reef health?
238
4. Do microbial community changes and host–microbe
interactions influence coral recovery and mortality
following disturbance?
5. Can changes in microbial community composition
mitigate ecosystem affects from environmental stress
and at what scales?
6. Do microbial community–host interactions influence
the ability of the host to withstand stressors?
7. Can we incorporate microbial communities into predictive models of coral reef ecosystem change?
Prosser [70] recently stated that quantitative information on the links between microbial community
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Trends in Ecology and Evolution
Vol.25 No.4
Figure 4. Microbial function impacts on ecosystem stability. Linkages between micro-ecology (microbial community dynamics) and macro-ecology on coral reefs (coral
community dynamics).
structure, populations and activities will allow predictions
on the impacts of climate change to microbial contributions
to ecosystem processes. In determining the future of coral
reefs worldwide we need to understand and incorporate
the complex role of microbial communities (Figure 4) as
systems that can respond to environmental change
within an ecological time frame and influence ecological
outcomes. The application of metagenomics provides a
means to answer many key questions that define the
relationship between microbial communities and environmentally driven macro-ecological change on reefs. Ultimately, this microbial perspective will improve our
ability to accurately predict the resilience of specific reefs
and contribute to the conservation of these important
ecosystems.
Acknowledgements
We thank Dr William Leggat and Dr Andrew Baird for extremely
valuable editorial assistance. The authors also thank funding sources
including; Edwin W. Pauley Foundation, Hawaii EPSCOR; The National
Science Foundation (OCE-0752604 to RDG); The National Science
Foundation research starter grant (IOS-0925454 to RLVT); and The
Australian Research Council, Australian Postdoctoral Fellowship
(DP0877226 to TDA). This manuscript represents Hawaii Institute for
Marine Biology contribution number 1373.
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