Patterns of ecological specialization among microbial populations in the Red Sea and diverse oligotrophic marine environments

Handle URI:
http://hdl.handle.net/10754/325398
Title:
Patterns of ecological specialization among microbial populations in the Red Sea and diverse oligotrophic marine environments
Authors:
Thompson, Luke R; Field, Chris; Romanuk, Tamara; Ngugi, David ( 0000-0002-0442-4279 ) ; Siam, Rania; El Dorry, Hamza; Stingl, Ulrich ( 0000-0002-0684-2597 )
Abstract:
Large swaths of the nutrient-poor surface ocean are dominated numerically by cyanobacteria (Prochlorococcus), cyanobacterial viruses (cyanophage), and alphaproteobacteria (SAR11). How these groups thrive in the diverse physicochemical environments of different oceanic regions remains poorly understood. Comparative metagenomics can reveal adaptive responses linked to ecosystem-specific selective pressures. The Red Sea is well-suited for studying adaptation of pelagic-microbes, with salinities, temperatures, and light levels at the extreme end for the surface ocean, and low nutrient concentrations, yet no metagenomic studies have been done there. The Red Sea (high salinity, high light, low N and P) compares favorably with the Mediterranean Sea (high salinity, low P), Sargasso Sea (low P), and North Pacific Subtropical Gyre (high light, low N). We quantified the relative abundance of genetic functions among Prochlorococcus, cyanophage, and SAR11 from these four regions. Gene frequencies indicate selection for phosphorus acquisition (Mediterranean/Sargasso), DNA repair and high-light responses (Red Sea/Pacific Prochlorococcus), and osmolyte C1 oxidation (Red Sea/Mediterranean SAR11). The unexpected connection between salinity-dependent osmolyte production and SAR11 C1 metabolism represents a potentially major coevolutionary adaptation and biogeochemical flux. Among Prochlorococcus and cyanophage, genes enriched in specific environments had ecotype distributions similar to nonenriched genes, suggesting that inter-ecotype gene transfer is not a major source of environment-specific adaptation. Clustering of metagenomes using gene frequencies shows similarities in populations (Red Sea with Pacific, Mediterranean with Sargasso) that belie their geographic distances. Taken together, the genetic functions enriched in specific environments indicate competitive strategies for maintaining carrying capacity in the face of physical stressors and low nutrient availability. 2013 The Authors. Ecology and Evolution.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Thompson LR, Field C, Romanuk T, Kamanda Ngugi D, Siam R, et al. (2013) Patterns of ecological specialization among microbial populations in the Red Sea and diverse oligotrophic marine environments. Ecology and Evolution 3: 1780-1797. doi:10.1002/ece3.593.
Publisher:
Wiley-Blackwell
Journal:
Ecology and Evolution
Issue Date:
11-May-2013
DOI:
10.1002/ece3.593
PubMed ID:
23789085
PubMed Central ID:
PMC3686209
Type:
Article
ISSN:
20457758
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Plankton Genomics, part of the Global Ocean Genome Project

Full metadata record

DC FieldValue Language
dc.contributor.authorThompson, Luke Ren
dc.contributor.authorField, Chrisen
dc.contributor.authorRomanuk, Tamaraen
dc.contributor.authorNgugi, Daviden
dc.contributor.authorSiam, Raniaen
dc.contributor.authorEl Dorry, Hamzaen
dc.contributor.authorStingl, Ulrichen
dc.date.accessioned2014-08-27T09:50:40Z-
dc.date.available2014-08-27T09:50:40Z-
dc.date.issued2013-05-11en
dc.identifier.citationThompson LR, Field C, Romanuk T, Kamanda Ngugi D, Siam R, et al. (2013) Patterns of ecological specialization among microbial populations in the Red Sea and diverse oligotrophic marine environments. Ecology and Evolution 3: 1780-1797. doi:10.1002/ece3.593.en
dc.identifier.issn20457758en
dc.identifier.pmid23789085en
dc.identifier.doi10.1002/ece3.593en
dc.identifier.urihttp://hdl.handle.net/10754/325398en
dc.description.abstractLarge swaths of the nutrient-poor surface ocean are dominated numerically by cyanobacteria (Prochlorococcus), cyanobacterial viruses (cyanophage), and alphaproteobacteria (SAR11). How these groups thrive in the diverse physicochemical environments of different oceanic regions remains poorly understood. Comparative metagenomics can reveal adaptive responses linked to ecosystem-specific selective pressures. The Red Sea is well-suited for studying adaptation of pelagic-microbes, with salinities, temperatures, and light levels at the extreme end for the surface ocean, and low nutrient concentrations, yet no metagenomic studies have been done there. The Red Sea (high salinity, high light, low N and P) compares favorably with the Mediterranean Sea (high salinity, low P), Sargasso Sea (low P), and North Pacific Subtropical Gyre (high light, low N). We quantified the relative abundance of genetic functions among Prochlorococcus, cyanophage, and SAR11 from these four regions. Gene frequencies indicate selection for phosphorus acquisition (Mediterranean/Sargasso), DNA repair and high-light responses (Red Sea/Pacific Prochlorococcus), and osmolyte C1 oxidation (Red Sea/Mediterranean SAR11). The unexpected connection between salinity-dependent osmolyte production and SAR11 C1 metabolism represents a potentially major coevolutionary adaptation and biogeochemical flux. Among Prochlorococcus and cyanophage, genes enriched in specific environments had ecotype distributions similar to nonenriched genes, suggesting that inter-ecotype gene transfer is not a major source of environment-specific adaptation. Clustering of metagenomes using gene frequencies shows similarities in populations (Red Sea with Pacific, Mediterranean with Sargasso) that belie their geographic distances. Taken together, the genetic functions enriched in specific environments indicate competitive strategies for maintaining carrying capacity in the face of physical stressors and low nutrient availability. 2013 The Authors. Ecology and Evolution.en
dc.language.isoenen
dc.publisherWiley-Blackwellen
dc.rights© 2013 Published by John Wiley & Sons Ltd.en
dc.rightsRe-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.en
dc.rightsArchived with thanks to Ecology and Evolutionen
dc.rights.urihttp://creativecommons.org/licenses/by/2.5/en
dc.subjectCyanophageen
dc.subjectMetagenomicsen
dc.subjectOsmolyteen
dc.subjectPelagibacteren
dc.subjectPopulation genomicsen
dc.subjectProchlorococcusen
dc.subjectSAR11en
dc.titlePatterns of ecological specialization among microbial populations in the Red Sea and diverse oligotrophic marine environmentsen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalEcology and Evolutionen
dc.identifier.pmcidPMC3686209en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionDepartment of Math and Statistics, Dalhousie University, Halifax, NS, B3H 3J5, Canadaen
dc.contributor.institutionDepartment of Biology, Dalhousie University, Halifax, NS, B3H 3J5, Canadaen
dc.contributor.institutionDepartment of Biology, The American University of Cairo, New Cairo, 11835, Egypten
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorThompson, Luke R.en
kaust.authorStingl, Ulrichen
kaust.authorNgugi, Daviden

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