Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton
Type
ArticleAuthors
Cardenas, AnnyNeave, Matthew J.
Haroon, Mohamed
Pogoreutz, Claudia
Radecker, Nils
Wild, Christian
Gärdes, Astrid
Voolstra, Christian R.

KAUST Department
Biological and Environmental Sciences and Engineering (BESE) DivisionMarine Science Program
Red Sea Research Center (RSRC)
Date
2017-09-12Permanent link to this record
http://hdl.handle.net/10754/625491
Metadata
Show full item recordAbstract
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.Citation
Cárdenas A, Neave MJ, Haroon MF, Pogoreutz C, Rädecker N, et al. (2017) Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton. The ISME Journal. Available: http://dx.doi.org/10.1038/ismej.2017.142.Sponsors
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.Publisher
Springer NatureJournal
The ISME JournalPubMed ID
28895945Additional Links
http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2017142a.htmlhttp://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2017142a.html
Relations
Is Supplemented By:- [Bioproject]
Title: Sugar enrichment effect on coral reef bacterioplanktonPublication Date: 2016-11-03. bioproject: PRJNA352340 Handle: 10754/666557
ae974a485f413a2113503eed53cd6c53
10.1038/ismej.2017.142
Scopus Count
Except where otherwise noted, this item's license is described as This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Related articles
- Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages.
- Authors: Nelson CE, Goldberg SJ, Wegley Kelly L, Haas AF, Smith JE, Rohwer F, Carlson CA
- Issue date: 2013 May
- Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity.
- Authors: Haas AF, Nelson CE, Wegley Kelly L, Carlson CA, Rohwer F, Leichter JJ, Wyatt A, Smith JE
- Issue date: 2011
- Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem.
- Authors: Nelson CE, Alldredge AL, McCliment EA, Amaral-Zettler LA, Carlson CA
- Issue date: 2011 Aug
- Global microbialization of coral reefs.
- Authors: Haas AF, Fairoz MF, Kelly LW, Nelson CE, Dinsdale EA, Edwards RA, Giles S, Hatay M, Hisakawa N, Knowles B, Lim YW, Maughan H, Pantos O, Roach TN, Sanchez SE, Silveira CB, Sandin S, Smith JE, Rohwer F
- Issue date: 2016 Apr 25
- Bacterioplankton drawdown of coral mass-spawned organic matter.
- Authors: Guillemette R, Kaneko R, Blanton J, Tan J, Witt M, Hamilton S, Allen EE, Medina M, Hamasaki K, Koch BP, Azam F
- Issue date: 2018 Sep