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      Ecosystem Microbiology of Coral Reefs: Linking Genomic, Metabolomic, and Biogeochemical Dynamics from Animal Symbioses to Reefscape Processes

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          Abstract

          Over the past 2 decades, molecular techniques have established the critical role of both free-living and host-associated microbial partnerships in the environment. Advancing research to link microbial community dynamics simultaneously to host physiology and ecosystem biogeochemistry is required to broaden our understanding of the ecological roles of environmental microbes.

          ABSTRACT

          Over the past 2 decades, molecular techniques have established the critical role of both free-living and host-associated microbial partnerships in the environment. Advancing research to link microbial community dynamics simultaneously to host physiology and ecosystem biogeochemistry is required to broaden our understanding of the ecological roles of environmental microbes. Studies on coral reefs are actively integrating these data streams at multiple levels, from the symbiotic habitat of the coral holobiont to microbially mediated interactions between corals and algae to the effects of these interactions on the microbial community structure, metabolism, and organic geochemistry of the reef ecosystem. Coral reefs endure multiple anthropogenic impacts, including pollution, overfishing, and global change. In this context, we must develop ecosystem microbiology with an eye to providing managers with microbial indicators of reef ecosystem processes, coral health, and resilience to both local and global stressors.

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          Most cited references13

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          Challenges in microbial ecology: building predictive understanding of community function and dynamics

          The importance of microbial communities (MCs) cannot be overstated. MCs underpin the biogeochemical cycles of the earth's soil, oceans and the atmosphere, and perform ecosystem functions that impact plants, animals and humans. Yet our ability to predict and manage the function of these highly complex, dynamically changing communities is limited. Building predictive models that link MC composition to function is a key emerging challenge in microbial ecology. Here, we argue that addressing this challenge requires close coordination of experimental data collection and method development with mathematical model building. We discuss specific examples where model–experiment integration has already resulted in important insights into MC function and structure. We also highlight key research questions that still demand better integration of experiments and models. We argue that such integration is needed to achieve significant progress in our understanding of MC dynamics and function, and we make specific practical suggestions as to how this could be achieved.
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            Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages.

            Increasing algal cover on tropical reefs worldwide may be maintained through feedbacks whereby algae outcompete coral by altering microbial activity. We hypothesized that algae and coral release compositionally distinct exudates that differentially alter bacterioplankton growth and community structure. We collected exudates from the dominant hermatypic coral holobiont Porites spp. and three dominant macroalgae (one each Ochrophyta, Rhodophyta and Chlorophyta) from reefs of Mo'orea, French Polynesia. We characterized exudates by measuring dissolved organic carbon (DOC) and fractional dissolved combined neutral sugars (DCNSs) and subsequently tracked bacterioplankton responses to each exudate over 48 h, assessing cellular growth, DOC/DCNS utilization and changes in taxonomic composition (via 16S rRNA amplicon pyrosequencing). Fleshy macroalgal exudates were enriched in the DCNS components fucose (Ochrophyta) and galactose (Rhodophyta); coral and calcareous algal exudates were enriched in total DCNS but in the same component proportions as ambient seawater. Rates of bacterioplankton growth and DOC utilization were significantly higher in algal exudate treatments than in coral exudate and control incubations with each community selectively removing different DCNS components. Coral exudates engendered the smallest shift in overall bacterioplankton community structure, maintained high diversity and enriched taxa from Alphaproteobacteria lineages containing cultured representatives with relatively few virulence factors (VFs) (Hyphomonadaceae and Erythrobacteraceae). In contrast, macroalgal exudates selected for less diverse communities heavily enriched in copiotrophic Gammaproteobacteria lineages containing cultured pathogens with increased VFs (Vibrionaceae and Pseudoalteromonadaceae). Our results demonstrate that algal exudates are enriched in DCNS components, foster rapid growth of bacterioplankton and select for bacterial populations with more potential VFs than coral exudates.
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              Global microbialization of coral reefs.

              Microbialization refers to the observed shift in ecosystem trophic structure towards higher microbial biomass and energy use. On coral reefs, the proximal causes of microbialization are overfishing and eutrophication, both of which facilitate enhanced growth of fleshy algae, conferring a competitive advantage over calcifying corals and coralline algae. The proposed mechanism for this competitive advantage is the DDAM positive feedback loop (dissolved organic carbon (DOC), disease, algae, microorganism), where DOC released by ungrazed fleshy algae supports copiotrophic, potentially pathogenic bacterial communities, ultimately harming corals and maintaining algal competitive dominance. Using an unprecedented data set of >400 samples from 60 coral reef sites, we show that the central DDAM predictions are consistent across three ocean basins. Reef algal cover is positively correlated with lower concentrations of DOC and higher microbial abundances. On turf and fleshy macroalgal-rich reefs, higher relative abundances of copiotrophic microbial taxa were identified. These microbial communities shift their metabolic potential for carbohydrate degradation from the more energy efficient Embden-Meyerhof-Parnas pathway on coral-dominated reefs to the less efficient Entner-Doudoroff and pentose phosphate pathways on algal-dominated reefs. This 'yield-to-power' switch by microorganism directly threatens reefs via increased hypoxia and greater CO2 release from the microbial respiration of DOC.
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                Author and article information

                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                13 March 2018
                Mar-Apr 2018
                : 3
                : 2
                : e00162-17
                Affiliations
                [a ]Department of Biology, San Diego State University, San Diego, California, USA
                [b ]Department of Marine Microbiology and Biogeochemistry, Royal NIOZ, the Netherlands Institute for Sea Research in cooperation with Utrecht University, Texel, Netherlands
                [c ]Center for Microbial Oceanography: Research and Education, Department of Oceanography and Sea Grant College Program, University of Hawai‘i at Mānoa, Honolulu, Hawai‘i, USA
                Author notes
                Address correspondence to Craig E. Nelson, craig.nelson@ 123456hawaii.edu .

                All authors contributed equally to this report.

                Conflict of Interest Disclosures: L.W.K. reports grant OCE-1538567 from the U.S. National Science Foundation during the conduct of the study. A.F.H. has nothing to disclose. C.E.N. reports grant OCE-1538393 from the U.S. National Science Foundation and grant NA14OAR4170071 from the National Oceanic and Atmospheric Administration during the conduct of the study.

                Citation Wegley Kelly L, Haas AF, Nelson CE. 2018. Ecosystem microbiology of coral reefs: linking genomic, metabolomic, and biogeochemical dynamics from animal symbioses to reefscape processes. mSystems 3:e00162-17. https://doi.org/10.1128/mSystems.00162-17.

                Author information
                https://orcid.org/0000-0003-2525-3496
                Article
                mSystems00162-17
                10.1128/mSystems.00162-17
                5850082
                aba14246-847a-4646-86d7-9446545e09db
                Copyright © 2018 Wegley Kelly et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 31 October 2017
                : 30 November 2017
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 15, Pages: 5, Words: 2980
                Categories
                Perspective
                Host-Microbe Biology
                Special Issue
                Custom metadata
                March/April 2018

                biogeochemistry,coral reef,ecosystem,metabolomics,metagenomics

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