Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton

Anny Cardenas, Matthew J. Neave, Mohamed Haroon, Claudia Pogoreutz, Nils Radecker, Christian Wild, Astrid Gärdes, Christian R. Voolstra

Research output: Contribution to journalArticlepeer-review

49 Scopus citations

Abstract

Coastal pollution and algal cover are increasing on many coral reefs, resulting in higher dissolved organic carbon (DOC) concentrations. High DOC concentrations strongly affect microbial activity in reef waters and select for copiotrophic, often potentially virulent microbial populations. High DOC concentrations on coral reefs are also hypothesized to be a determinant for switching microbial lifestyles from commensal to pathogenic, thereby contributing to coral reef degradation, but evidence is missing. In this study, we conducted ex situ incubations to assess gene expression of planktonic microbial populations under elevated concentrations of naturally abundant monosaccharides (glucose, galactose, mannose, and xylose) in algal exudates and sewage inflows. We assembled 27 near-complete (>70%) microbial genomes through metagenomic sequencing and determined associated expression patterns through metatranscriptomic sequencing. Differential gene expression analysis revealed a shift in the central carbohydrate metabolism and the induction of metalloproteases, siderophores, and toxins in Alteromonas, Erythrobacter, Oceanicola, and Alcanivorax populations. Sugar-specific induction of virulence factors suggests a mechanistic link for the switch from a commensal to a pathogenic lifestyle, particularly relevant during increased algal cover and human-derived pollution on coral reefs. Although an explicit test remains to be performed, our data support the hypothesis that increased availability of specific sugars changes net microbial community activity in ways that increase the emergence and abundance of opportunistic pathogens, potentially contributing to coral reef degradation.
Original languageEnglish (US)
Pages (from-to)59-76
Number of pages18
JournalThe ISME Journal
Volume12
Issue number1
DOIs
StatePublished - Sep 12 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Till Röthig and Anna Roik for their assistance during water collection, Craig Michell and Camille Daniels for their assistance during nucleic acids isolation and sequencing libraries preparation, Sebastian Baumgarten for his support with bioinformatics resources. We further thank the editor and four anonymous reviewers for their constructive comments, which greatly improved the manuscript. Research reported in this publication was funded by the King Abdullah University of Science and Technology (KAUST) and Leibniz Center for Tropical Marine Ecology (ZMT) grants. AC acknowledges financial support by the Leibnitz Center for Tropical Marine Ecology and International Max Planck Research School of Marine Microbiology (MarMic). The contribution of CP was supported by GLOMAR—Bremen International Graduate School for Marine Sciences.

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