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Global microbialization of coral reefs

Nature Microbiology volume 1, Article number: 16042 (2016) Cite this article

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Abstract

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.

As the world's most productive and diverse marine ecosystems, coral reefs have a wide variety of mechanisms for cycling energy and nutrients. Benthic primary producers, namely zooxanthellae-harbouring corals and crustose coralline algae (CCA), form the base of the pristine coral reef food web1. In addition to direct trophic transfer of primary production through herbivory, a number of processes recycle organic matter in reef ecosystems.

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Figure 1: Sampling sites.
Figure 2: Algal cover compared to DOC and microbial abundance.
Figure 3: Metagenomic taxonomic and functional analysis of reef-associated microbial communities.

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Acknowledgements

Reef water samples were collected during two research expeditions to the Line Islands funded by the National Geographic Society, the Moore Family Foundation, the Fairweather Foundation, the Marine Managed Areas Science Project of Conservation International, Scripps Institution of Oceanography, E. Scripps, I. Gayler and several private donors. The authors thank the captain and crew of the RV White Holly and MV ‘Searcher’ for logistical support and hospitality. Field support was also provided by S. Ahamed and the Co-operative Society of Tourist Boat Operators, Pigion Island, in Sri Lanka. This work was carried out under research permits from the US Fish and Wildlife Service to operate in the Kingman Atoll National Wildlife Refuge and the Environment and Conservation Division of the Republic of Kiribati. The authors thank The Nature Conservancy and the Palmyra Atoll Research Consortium for additional field support. This research was sponsored by the Marine Microbial Initiative of the Gordon and Betty Moore Foundation and by GBMF Investigator Award 3781 as well as a Canadian Institute for Advanced Research Integrated Microbial Biodiversity Program Fellowship 141679 and the Pew Charitable Trusts award MASTER 666/PROJ 28972 (to F.R.). It was funded by the US National Science Foundation awards OCE–1538567 (to L.W.K.), OCE–1538393 (to C.E.N.) and DUE–1323809 (to E.A.D.). C.E.N. was funded in part by a grant/cooperative agreement from the National Oceanic and Atmospheric Administration, Project A/AS-1, which is sponsored by the University of Hawaii Sea Grant College Program, SOEST, under Institutional Grant No. NA14OAR4170071 from NOAA Office of Sea Grant, Department of Commerce. The views expressed herein are those of the author(s) and do not necessarily reflect the views of NOAA or any of its subagencies. This manuscript is UH SOEST publication no. 9575 and UH Sea Grant publication number UNIHI-SEAGRANT-JC-15-12. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Author notes

  1. Andreas F. Haas and Mohamed F. M. Fairoz: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, San Diego State University, San Diego, 92182, California, USA

    Andreas F. Haas, Linda W. Kelly, Elizabeth A. Dinsdale, Robert A. Edwards, Mark Hatay, Nao Hisakawa, Ben Knowles, Yan Wei Lim, Ty N. F. Roach, Savannah E. Sanchez, Cynthia B. Silveira & Forest Rohwer

  2. Faculty of Fisheries and Marine Sciences, Ocean University of Sri Lanka, Tangalle, Sri Lanka

    Mohamed F. M. Fairoz

  3. Department of Oceanography and Sea Grant College Program, Center for Microbial Oceanography: Research and Education, School of Ocean and Earth Science and Technology, University of Hawaiʻi at Mānoa, Hawaii 96822, USA

    Craig E. Nelson

  4. Big Rose Web Design, 8550 Greenway Blvd, LLC, Madison, 53562, Wisconsin, USA

    Steve Giles

  5. Ronin Institute, Montclair, 07043, New Jersey, USA

    Heather Maughan

  6. Global Change Institute, University of Queensland, St Lucia, 4072, Queensland, Australia

    Olga Pantos

  7. Scripps Institution of Oceanography, University of California San Diego, La Jolla, 92093, California, USA

    Stuart Sandin & Jennifer E. Smith

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  1. Andreas F. Haas
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Contributions

A.F.H., M.F.M.F., L.W.K. and C.E.N. conceptualized the study, analysed data and wrote the paper. E.A.D., R.A.E., S.G., M.H., N.H., B.K., Y.W.L., H.M., O.P., T.N.F.R., S.E.S., C.B.S., S.S. and J.E.S. performed experiments and analysed data. F.R. contributed to the concept and design of the study, data analysis and manuscript writing.

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Correspondence to Andreas F. Haas.

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Supplementary Figures 1-3 and Tables 1-4. (PDF 703 kb)

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Haas, A., Fairoz, M., Kelly, L. et al. Global microbialization of coral reefs. Nat Microbiol 1, 16042 (2016). https://doi.org/10.1038/nmicrobiol.2016.42

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