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Biophysical and physiological causes of coral reef microbialization

View ORCID ProfileCynthia B. Silveira, Ty N. F. Roach, Helena Villela, Adam Barno, Brandon Reyes, Esther Rubio-Portillo, Tram Le, Spencer Mead, Mark Hatay, Antoni Luque, Linda Wegley-Kelly, Mark Vermeij, Barbara Bailey, Yui Takeshita, Andreas Haas, Forest Rohwer
doi: https://doi.org/10.1101/495481
Cynthia B. Silveira
1Department of Biology, San Diego State University, San Diego, CA, USA
2Viral Information Institute, San Diego State University, San Diego, CA, USA
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  • ORCID record for Cynthia B. Silveira
Ty N. F. Roach
1Department of Biology, San Diego State University, San Diego, CA, USA
2Viral Information Institute, San Diego State University, San Diego, CA, USA
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Helena Villela
1Department of Biology, San Diego State University, San Diego, CA, USA
3Department of Microbiology, Rio de Janeiro Federal University, Rio de Janeiro, Brazil
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Adam Barno
1Department of Biology, San Diego State University, San Diego, CA, USA
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Brandon Reyes
1Department of Biology, San Diego State University, San Diego, CA, USA
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Esther Rubio-Portillo
1Department of Biology, San Diego State University, San Diego, CA, USA
4Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain
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Tram Le
1Department of Biology, San Diego State University, San Diego, CA, USA
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Spencer Mead
1Department of Biology, San Diego State University, San Diego, CA, USA
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Mark Hatay
1Department of Biology, San Diego State University, San Diego, CA, USA
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Antoni Luque
5Department of Mathematics & Statistics, San Diego State University, San Diego, CA, USA
2Viral Information Institute, San Diego State University, San Diego, CA, USA
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Linda Wegley-Kelly
1Department of Biology, San Diego State University, San Diego, CA, USA
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Mark Vermeij
6CARMABI Foundation, Willemstad, Curaçao
7Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands
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Barbara Bailey
5Department of Mathematics & Statistics, San Diego State University, San Diego, CA, USA
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Yui Takeshita
8Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA
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Andreas Haas
9NIOZ Royal Netherlands Institute for Sea Research and Utrecht University, Texel, The Netherlands
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Forest Rohwer
1Department of Biology, San Diego State University, San Diego, CA, USA
2Viral Information Institute, San Diego State University, San Diego, CA, USA
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Abstract

Coral reefs are declining globally as their primary producer communities shift from stony coral to fleshy macroalgae dominance. Previously, we have shown that the rise of fleshy macroalgae produces dissolved organic carbon (DOC) that lead to microbialization and coral death. Here we test the hypothesis that the biophysical cause of bacterial biomass accumulation is a relative decrease in electron acceptors relative to electron donors due to O2 loss from macroalgae. We show that 37 % of photosynthetic O2 produced by reef fleshy macroalgae is lost in the form of gas through ebullition from algae surfaces. O2 loss increases DOC:O2 ratios, decoupling the photosynthetically fixed carbon from oxidative potential for respiration. This biogeochemical environment drives heterotrophic microbes to increase cell-specific DOC consumption and cell sizes, accumulating biomass. In contrast, corals do not lose oxygen and support the growth of smaller and fewer bacteria. In situ biomass and metagenomic analyses of 87 reefs across the Pacific and Caribbean show that on algae-dominated reefs bacteria accumulate organic carbon through a Warburg-like increase in aerobic glycolytic metabolism. Because of its biophysical basis, microbialization is predicted to occur in other marine ecosystems shifting primary producer assemblages, such as planktonic communities in warming and acidifying conditions.

Footnotes

  • Statement of authorship: CBS, BR, LWK, MH, MV, YT, AH and FR designed experiments and sampling; CBS, TR, HV, BR, ERP, AL, MV, and AH performed experiments; CBS, TR, AB, TL, and SM generated microscopy and metagenomic data; CBS and BB performed statistical analyses; CS wrote the manuscript and all authors contributed substantially with revisions.

  • Data availability Statement Experimental data are provided as supporting datasets and in FigShare (https://doi.org/10.6084/m9.figshare.7170254.v1). Metagenomic data are available in the NCBI SRA under PRJNA494971.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 13, 2018.
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Biophysical and physiological causes of coral reef microbialization
Cynthia B. Silveira, Ty N. F. Roach, Helena Villela, Adam Barno, Brandon Reyes, Esther Rubio-Portillo, Tram Le, Spencer Mead, Mark Hatay, Antoni Luque, Linda Wegley-Kelly, Mark Vermeij, Barbara Bailey, Yui Takeshita, Andreas Haas, Forest Rohwer
bioRxiv 495481; doi: https://doi.org/10.1101/495481
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Biophysical and physiological causes of coral reef microbialization
Cynthia B. Silveira, Ty N. F. Roach, Helena Villela, Adam Barno, Brandon Reyes, Esther Rubio-Portillo, Tram Le, Spencer Mead, Mark Hatay, Antoni Luque, Linda Wegley-Kelly, Mark Vermeij, Barbara Bailey, Yui Takeshita, Andreas Haas, Forest Rohwer
bioRxiv 495481; doi: https://doi.org/10.1101/495481

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