Global microbialization of coral reefs

  • Nature Microbiology 1, Article number: 16042 (2016)
  • doi:10.1038/nmicrobiol.2016.42
  • Download Citation
Published online:


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.

  • Subscribe to Nature Microbiology for full access:



Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.


  1. 1.

    et al. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428, 66–70 (2004).

  2. 2.

    et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342, 108–110 (2013).

  3. 3.

    et al. Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PLoS ONE 6, e27973 (2011).

  4. 4.

    et al. Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J. 7, 962–979 (2013).

  5. 5.

    in Biogeochemistry of Marine Dissolved Organic Matter (eds Hansell, D. A. & Carlson, C. A.) 123–124 (Academic, 2014).

  6. 6.

    & Localized refractory dissolved organic carbon sinks in the deep ocean. Glob. Biogeochem. Cycles 27, 20067 (2013).

  7. 7.

    ‘Coral dominance’: a dangerous ecosystem misnomer? J. Mar. Biol. 2011, 164127 (2011).

  8. 8.

    et al. Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 3, e1548 (2008).

  9. 9.

    et al. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17, 360–365 (2007).

  10. 10.

    , & Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 (2000).

  11. 11.

    , , , & Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl Acad. Sci. USA 105, 17442–17446 (2008).

  12. 12.

    et al. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc. Natl Acad. Sci. USA 105, 18413–18418 (2008).

  13. 13.

    et al. Microbial ecology of four coral atolls in the northern Line Islands. PLoS ONE 3, 1584 (2008).

  14. 14.

    et al. Black reefs: iron induced phase-shift on coral reefs. ISME J. 6, 638–649 (2012).

  15. 15.

    , , & Organic matter release by Red Sea coral reef organisms—potential effects on microbial activity and in-situ O2 availability. Mar. Ecol. Prog. Ser. 411, 61–71 (2010).

  16. 16.

    , , , & Organic matter release by the dominant primary producers in a Caribbean reef lagoon: implication for in-situ O2 availability. Mar. Ecol. Prog. Ser. 409, 27–39 (2010).

  17. 17.

    et al. Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms. Coral Reefs 30, 309–320 (2011).

  18. 18.

    et al. Influence of coral and algal exudates on microbially mediated reef metabolism. PeerJ 1, e108 (2013).

  19. 19.

    , , , & Role of elevated organic carbon levels and microbial activity in coral mortality. Mar. Ecol. Prog. Ser. 314, 119–125 (2006).

  20. 20.

    et al. Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol. Lett. 9, 835–845 (2006).

  21. 21.

    et al. Pathologies and mortality rates caused by organic carbon and nutrient stressors in three Caribbean coral species. Mar. Ecol. Prog. Ser. 294, 173–180 (2005).

  22. 22.

    & Unseen players shape benthic competition on coral reefs. Trends Microbiol. 20, 621–628 (2012).

  23. 23.

    , & Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19, 400–417 (2001).

  24. 24.

    et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).

  25. 25.

    , , , & Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem. ISME J. 5, 1374–1387 (2011).

  26. 26.

    et al. Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455, 387–390 (2008).

  27. 27.

    Comparison of mechanisms enhancing biodegradability of refractory lake water constituents. Limnol. Oceanogr. 31, 755–764 (1986).

  28. 28.

    et al. Seafloor ecosystem functioning: the importance of organic matter priming. Mar. Biol. 156, 2277–2287 (2009).

  29. 29.

    , & Consumption of dissolved organic carbon by marine bacteria and demand for inorganic nutrients. Mar. Ecol. Prog. Ser. 101, 23–32 (1993).

  30. 30.

    , & Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385, 148–151 (1997).

  31. 31.

    , & in Microbial Carbon Pump in the Ocean (eds Jiao, N., Azam, F. & Sanders, S.) 54–56 (AAAS, 2011).

  32. 32.

    & Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol. Evol. 13, 316–321 (1998).

  33. 33.

    & KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).

  34. 34.

    et al. The genomic basis of trophic strategy in marine bacteria. Proc. Natl Acad. Sci. USA 106, 15527–15533 (2009).

  35. 35.

    et al. Emerging marine diseases—climate links and anthropogenic factors. Science 285, 1505–1510 (1999).

  36. 36.

    & Bacterial Physiology and Metabolism (Cambridge Univ. Press, 2008).

  37. 37.

    & Evolution of carbohydrate metabolic pathways. Res. Microbiol. 147, 448–455 (1996).

  38. 38.

    , , , & Glycolytic strategy as a tradeoff between energy yield and protein cost. Proc. Natl Acad. Sci. USA 110, 10039–10044 (2013).

  39. 39.

    , & Thermodynamic efficiency of microbial growth is low but optimal for maximal growth rate. Proc. Natl Acad. Sci. USA 80, 305–309 (1983).

  40. 40.

    & The cost of efficiency in energy metabolism. Proc. Natl Acad. Sci. USA 110, 9629–9630 (2013).

  41. 41.

    & Game-theoretical approaches to studying the evolution of biochemical systems. Trends Biochem. Sci. 30, 20–25 (2005).

  42. 42.

    & Time speed regulator: the optimum efficiency for the maximum power output in physical and biological systems. Am. Sci. 43, 331–343 (1955).

  43. 43.

    Mutants of the pentose phosphate pathway in Aspergillus nidulans. J. Bacteriol. 117, 1121–1130 (1974).

  44. 44.

    Genetics of pentose-phosphate pathway enzymes of Escherichia coli K-12. Arch. Microbiol. 164, 324–330 (1995).

  45. 45.

    & Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat. Biol. 10, 131–138 (2010).

  46. 46.

    in Algal Culture from Laboratory to Pilot Plant Vol. 600 (ed., Burlew, J. F.) 285–302 (Carnegie Institution of Washington, 1953).

  47. 47.

    et al. Assessing coral reefs on a Pacific-wide scale using the microbialization score. PLoS ONE 7, e43233 (2012).

  48. 48.

    et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).

  49. 49.

    , & Will ocean acidification affect marine microbes? ISME J. 5, 1–7 (2011).

  50. 50.

    , , & Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs. PLoS ONE 7, e43843 (2012).

  51. 51.

    , & A rapid ecological assessment (REA) quantitative survey method for benthic algae using photo quadrats with SCUBA. Pacif. Sci. 58, 201–209 (2004).

  52. 52.

    et al. Unraveling the unseen players in the ocean—a field guide to water chemistry and marine microbiology. J. Vis. Exp. 93, e52131 (2014).

  53. 53.

    et al. Final dissolved organic carbon broad community intercalibration and preliminary use of DOC reference materials. Mar. Chem. 77, 239–253 (2002).

  54. 54.

    , , & Dissolved organic matter in the ocean: a controversy stimulates new insights. Oceanography 22, 202–211 (2009).

  55. 55.

    et al. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc. Natl Acad. Sci. USA 111, 10227–10232 (2014).

  56. 56.

    & Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863–864 (2011).

  57. 57.

    et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).

  58. 58.

    et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput. Biol. 8, e1002358 (2012).

  59. 59.

    et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res. 33, 325–328 (2005).

  60. 60.

    , & The Analysis of Means: A Graphical Method for Comparing Means, Rates, and Proportions (SIAM, 2005).

Download references


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.

Author information

Author notes

    • Andreas F. Haas
    •  & Mohamed F. M. Fairoz

    These authors contributed equally to this work.


  1. Department of Biology, San Diego State University, San Diego, California 92182, 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. Center for Microbial Oceanography: Research and Education, Department of Oceanography and Sea Grant College Program, 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, Wisconsin 53562, USA

    • Steve Giles
  5. Ronin Institute, Montclair, New Jersey 07043, USA

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

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

    • Stuart Sandin
    •  & Jennifer E. Smith


  1. Search for Andreas F. Haas in:

  2. Search for Mohamed F. M. Fairoz in:

  3. Search for Linda W. Kelly in:

  4. Search for Craig E. Nelson in:

  5. Search for Elizabeth A. Dinsdale in:

  6. Search for Robert A. Edwards in:

  7. Search for Steve Giles in:

  8. Search for Mark Hatay in:

  9. Search for Nao Hisakawa in:

  10. Search for Ben Knowles in:

  11. Search for Yan Wei Lim in:

  12. Search for Heather Maughan in:

  13. Search for Olga Pantos in:

  14. Search for Ty N. F. Roach in:

  15. Search for Savannah E. Sanchez in:

  16. Search for Cynthia B. Silveira in:

  17. Search for Stuart Sandin in:

  18. Search for Jennifer E. Smith in:

  19. Search for Forest Rohwer in:


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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Andreas F. Haas.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1-3 and Tables 1-4.