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

Handle URI:
http://hdl.handle.net/10754/625491
Title:
Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton
Authors:
Cardenas, Anny; Neave, Matthew J; Haroon, Mohamed; Pogoreutz, Claudia; Radecker, Nils; Wild, Christian; Gärdes, Astrid; Voolstra, Christian R. ( 0000-0003-4555-3795 )
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.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC)
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.
Publisher:
Springer Nature
Journal:
The ISME Journal
Issue Date:
12-Sep-2017
DOI:
10.1038/ismej.2017.142
Type:
Article
ISSN:
1751-7362; 1751-7370
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.
Additional Links:
http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2017142a.html; http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2017142a.html
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorCardenas, Annyen
dc.contributor.authorNeave, Matthew Jen
dc.contributor.authorHaroon, Mohameden
dc.contributor.authorPogoreutz, Claudiaen
dc.contributor.authorRadecker, Nilsen
dc.contributor.authorWild, Christianen
dc.contributor.authorGärdes, Astriden
dc.contributor.authorVoolstra, Christian R.en
dc.date.accessioned2017-09-21T09:25:33Z-
dc.date.available2017-09-21T09:25:33Z-
dc.date.issued2017-09-12en
dc.identifier.citationCárdenas 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.en
dc.identifier.issn1751-7362en
dc.identifier.issn1751-7370en
dc.identifier.doi10.1038/ismej.2017.142en
dc.identifier.urihttp://hdl.handle.net/10754/625491-
dc.description.abstractCoastal 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.en
dc.description.sponsorshipWe 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.en
dc.publisherSpringer Natureen
dc.relation.urlhttp://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2017142a.htmlen
dc.relation.urlhttp://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2017142a.htmlen
dc.rightsThis 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/.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleExcess labile carbon promotes the expression of virulence factors in coral reef bacterioplanktonen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalThe ISME Journalen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionMax Plank Institute for Marine Microbiology, Bremen, Germanyen
dc.contributor.institutionLeibniz Center for Tropical Marine Ecology (ZMT), Bremen, Germanyen
dc.contributor.institutionDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USAen
dc.contributor.institutionDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.en
dc.contributor.institutionMarine Ecology Group, Faculty of Biology and Chemistry, University of Bremen, Germanyen
dc.contributor.institutionMarine Ecology Group, Faculty of Biology and Chemistry, University of Bremen, Germany.en
dc.contributor.institutionLeibniz Center for Tropical Marine Ecology (ZMT), Bremen, Germany.en
kaust.authorCardenas, Annyen
kaust.authorNeave, Matthew Jen
kaust.authorHaroon, Mohameden
kaust.authorPogoreutz, Claudiaen
kaust.authorRadecker, Nilsen
kaust.authorVoolstra, Christian R.en
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