Combined analyses of the ITS loci and the corresponding 16S rRNA genes reveal high micro- and macrodiversity of SAR11 populations in the Red Sea.

Handle URI:
http://hdl.handle.net/10754/323506
Title:
Combined analyses of the ITS loci and the corresponding 16S rRNA genes reveal high micro- and macrodiversity of SAR11 populations in the Red Sea.
Authors:
Ngugi, David ( 0000-0002-0442-4279 ) ; Stingl, Ulrich ( 0000-0002-0684-2597 )
Abstract:
Bacteria belonging to the SAR11 clade are among the most abundant prokaryotes in the pelagic zone of the ocean. 16S rRNA gene-based analyses indicate that they constitute up to 60% of the bacterioplankton community in the surface waters of the Red Sea. This extremely oligotrophic water body is further characterized by an epipelagic zone, which has a temperature above 24 °C throughout the year, and a remarkable uniform temperature (~22 °C) and salinity (~41 psu) from the mixed layer (~200 m) to the bottom at over 2000 m depth. Despite these conditions that set it apart from other marine environments, the microbiology of this ecosystem is still vastly understudied. Prompted by the limited phylogenetic resolution of the 16S rRNA gene, we extended our previous study by sequencing the internal transcribed spacer (ITS) region of SAR11 in different depths of the Red Sea's water column together with the respective 16S fragment. The overall diversity captured by the ITS loci was ten times higher than that of the corresponding 16S rRNA genes. Moreover, species estimates based on the ITS showed a highly diverse population of SAR11 in the mixed layer that became diminished in deep isothermal waters, which was in contrast to results of the related 16S rRNA genes. While the 16S rRNA gene-based sequences clustered into three phylogenetic subgroups, the related ITS fragments fell into several phylotypes that showed clear depth-dependent shifts in relative abundances. Blast-based analyses not only documented the observed vertical partitioning and universal co-occurrence of specific phylotypes in five other distinct oceanic provinces, but also highlighted the influence of ecosystem-specific traits (e.g., temperature, nutrient availability, and concentration of dissolved oxygen) on the population dynamics of this ubiquitous marine bacterium.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Ngugi DK, Stingl U (2012) Combined Analyses of the ITS Loci and the Corresponding 16S rRNA Genes Reveal High Micro- and Macrodiversity of SAR11 Populations in the Red Sea. PLoS ONE 7: e50274. doi:10.1371/journal.pone.0050274.
Publisher:
Public Library of Science (PLoS)
Journal:
PLoS ONE
Issue Date:
20-Nov-2012
DOI:
10.1371/journal.pone.0050274
PubMed ID:
23185592
PubMed Central ID:
PMC3502338
Type:
Article
ISSN:
1932-6203
Additional Links:
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0050274; http://europepmc.org/articles/PMC3502338
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.authorNgugi, Daviden
dc.contributor.authorStingl, Ulrichen
dc.date.accessioned2014-07-21T10:15:10Z-
dc.date.available2014-07-21T10:15:10Z-
dc.date.issued2012-11-20en
dc.identifier.citationNgugi DK, Stingl U (2012) Combined Analyses of the ITS Loci and the Corresponding 16S rRNA Genes Reveal High Micro- and Macrodiversity of SAR11 Populations in the Red Sea. PLoS ONE 7: e50274. doi:10.1371/journal.pone.0050274.en
dc.identifier.issn1932-6203en
dc.identifier.pmid23185592en
dc.identifier.doi10.1371/journal.pone.0050274en
dc.identifier.urihttp://hdl.handle.net/10754/323506en
dc.description.abstractBacteria belonging to the SAR11 clade are among the most abundant prokaryotes in the pelagic zone of the ocean. 16S rRNA gene-based analyses indicate that they constitute up to 60% of the bacterioplankton community in the surface waters of the Red Sea. This extremely oligotrophic water body is further characterized by an epipelagic zone, which has a temperature above 24 °C throughout the year, and a remarkable uniform temperature (~22 °C) and salinity (~41 psu) from the mixed layer (~200 m) to the bottom at over 2000 m depth. Despite these conditions that set it apart from other marine environments, the microbiology of this ecosystem is still vastly understudied. Prompted by the limited phylogenetic resolution of the 16S rRNA gene, we extended our previous study by sequencing the internal transcribed spacer (ITS) region of SAR11 in different depths of the Red Sea's water column together with the respective 16S fragment. The overall diversity captured by the ITS loci was ten times higher than that of the corresponding 16S rRNA genes. Moreover, species estimates based on the ITS showed a highly diverse population of SAR11 in the mixed layer that became diminished in deep isothermal waters, which was in contrast to results of the related 16S rRNA genes. While the 16S rRNA gene-based sequences clustered into three phylogenetic subgroups, the related ITS fragments fell into several phylotypes that showed clear depth-dependent shifts in relative abundances. Blast-based analyses not only documented the observed vertical partitioning and universal co-occurrence of specific phylotypes in five other distinct oceanic provinces, but also highlighted the influence of ecosystem-specific traits (e.g., temperature, nutrient availability, and concentration of dissolved oxygen) on the population dynamics of this ubiquitous marine bacterium.en
dc.language.isoenen
dc.publisherPublic Library of Science (PLoS)en
dc.relation.urlhttp://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0050274en
dc.relation.urlhttp://europepmc.org/articles/PMC3502338en
dc.rightsArchived with thanks to PloS oneen
dc.subject.meshAlphaproteobacteriaen
dc.subject.meshBase Sequenceen
dc.subject.meshBiodiversityen
dc.subject.meshDNA, Bacterialen
dc.subject.meshDNA, Intergenicen
dc.subject.meshEcosystemen
dc.subject.meshGenetic Locien
dc.subject.meshIndian Oceanen
dc.subject.meshMolecular Sequence Dataen
dc.subject.meshPhylogenyen
dc.subject.meshPlanktonen
dc.subject.meshRNA, Ribosomal, 16Sen
dc.subject.meshSalinityen
dc.subject.meshTemperatureen
dc.subject.meshAlphaproteobacteriaen
dc.subject.meshBase Sequenceen
dc.subject.meshBiodiversityen
dc.subject.meshDNA, Bacterialen
dc.subject.meshDNA, Intergenicen
dc.subject.meshEcosystemen
dc.subject.meshGenetic Locien
dc.subject.meshIndian Oceanen
dc.subject.meshMolecular Sequence Dataen
dc.subject.meshPhylogenyen
dc.subject.meshPlanktonen
dc.subject.meshRNA, Ribosomal, 16Sen
dc.subject.meshSalinityen
dc.subject.meshTemperatureen
dc.titleCombined analyses of the ITS loci and the corresponding 16S rRNA genes reveal high micro- and macrodiversity of SAR11 populations in the Red Sea.en
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalPLoS ONEen
dc.identifier.pmcidPMC3502338en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionBiotechnology Graduate Program, American University in Cairo, Cairo, Egypten
dc.contributor.institutionDepartment of Biology, American University in Cairo, Cairo, Egypten
dc.contributor.institutionThe Science and Technology Research Center, American University in Cairo, Cairo, Egypten
dc.contributor.institutionDepartment of Chemistry, American University in Cairo, Cairo, Egypten
dc.contributor.institutionMarine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United Statesen
dc.contributor.institutionJosephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA, United Statesen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorNgugi, Daviden
kaust.authorStingl, Ulrichen

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  • Files 10

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      Article - PLoS ONE -...
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      Article - Full Text
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      Figure_S1.pdf
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      Figure S1 - Physicochemical parameters in the water column of central Red Sea
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      Figure_S2.pdf
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      Figure S2 - Rarefaction curves for (A) 16S rRNA gene sequences and (B) the related ITS fragments in our clone libraries.
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      Figure_S3.pdf
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      Figure S3 - Principal coordinate analysis (PCoA) showing the clustering of SAR11 populations in the different samples based on the weighted UniFrac distance metric for both 16S rRNA genes and ITS sequences.
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      Figure_S4.pdf
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      Phylogeny of 16S rRNA genes generated in our study.
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      Figure_S5.pdf
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      Phylogenetic tree showing the position of the corresponding ITS fragments.
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      Table_S1.pdf
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      Table S1 - Environmental and physicochemical traits of seawater samples used for clone libraries in our study.
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      Table_S2.pdf
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      Table S2 - Identity of the major OTUs in our clone libraries (with an abundance of >1%) based on the 16S rRNA gene, relative to each other and to cultivated strains within the SAR11 clade.
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      Table_S3.xlsx
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      Table S3 - Metagenomic libraries and their associated metadata that were used to recruit various SAR11-specific ITS reads and 16S rRNA gene sequences homologous to those in our annotated reference databases.
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      Table_S4.pdf
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      Table S4 - Sample pairs with significant differences in phylotype composition based on Phylogenetic/Parsimony (P) test.
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