Genomic repertoire of the Woeseiaceae/JTB255, cosmopolitan and abundant core members of microbial communities in marine sediments

To date, very little is known about the bacterial core community of marine sediments. Here we study the environmental distribution, abundance and ecogenomics of the gammaproteobacterial Woeseiaceae /JTB255 marine benthic group. A meta-analysis of published work shows that the Woeseiaceae /JTB255 are...

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Published in:	The ISME Journal Vol. 11; no. 5; pp. 1276 - 1281
Main Authors:	Mußmann, Marc, Pjevac, Petra, Krüger, Karen, Dyksma, Stefan
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 01.05.2017 Oxford University Press Nature Publishing Group
Subjects:	14/32 14/63 45/23 631/326/171/1878 704/158/855 Australia Autotrophic Processes Biomedical and Life Sciences Ecological function Ecology Evolutionary Biology Gammaproteobacteria - classification Gammaproteobacteria - genetics Gammaproteobacteria - isolation & purification Gammaproteobacteria - metabolism Genome, Bacterial Geologic Sediments - microbiology Heterotrophic Processes Life Sciences Marine sediments Metagenomics Microbial activity Microbial Ecology Microbial Genetics and Genomics Microbiology Nitrous oxide Oceans and Seas Phylogeny RNA, Ribosomal, 16S - genetics Short Communication Australia
ISSN:	1751-7362, 1751-7370
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Abstract	To date, very little is known about the bacterial core community of marine sediments. Here we study the environmental distribution, abundance and ecogenomics of the gammaproteobacterial Woeseiaceae /JTB255 marine benthic group. A meta-analysis of published work shows that the Woeseiaceae /JTB255 are ubiquitous and consistently rank among the most abundant 16S rRNA gene sequences in diverse marine sediments. They account for up to 22% of bacterial amplicons and 6% of total cell counts in European and Australian coastal sediments. The analysis of a single-cell genome, metagenomic bins and the genome of the next cultured relative Woeseia oceani indicated a broad physiological range, including heterotrophy and facultative autotrophy. All tested (meta)genomes encode a truncated denitrification pathway to nitrous oxide. The broad range of energy-yielding metabolisms possibly explains the ubiquity and high abundance of Woeseiaceae /JTB255 in marine sediments, where they carry out diverse, but yet unknown ecological functions.
AbstractList	To date, very little is known about the bacterial core community of marine sediments. Here we study the environmental distribution, abundance and ecogenomics of the gammaproteobacterial Woeseiaceae/JTB255 marine benthic group. A meta-analysis of published work shows that the Woeseiaceae/JTB255 are ubiquitous and consistently rank among the most abundant 16S rRNA gene sequences in diverse marine sediments. They account for up to 22% of bacterial amplicons and 6% of total cell counts in European and Australian coastal sediments. The analysis of a single-cell genome, metagenomic bins and the genome of the next cultured relative Woeseia oceani indicated a broad physiological range, including heterotrophy and facultative autotrophy. All tested (meta)genomes encode a truncated denitrification pathway to nitrous oxide. The broad range of energy-yielding metabolisms possibly explains the ubiquity and high abundance of Woeseiaceae/JTB255 in marine sediments, where they carry out diverse, but yet unknown ecological functions. To date, very little is known about the bacterial core community of marine sediments. Here we study the environmental distribution, abundance and ecogenomics of the gammaproteobacterial Woeseiaceae /JTB255 marine benthic group. A meta-analysis of published work shows that the Woeseiaceae /JTB255 are ubiquitous and consistently rank among the most abundant 16S rRNA gene sequences in diverse marine sediments. They account for up to 22% of bacterial amplicons and 6% of total cell counts in European and Australian coastal sediments. The analysis of a single-cell genome, metagenomic bins and the genome of the next cultured relative Woeseia oceani indicated a broad physiological range, including heterotrophy and facultative autotrophy. All tested (meta)genomes encode a truncated denitrification pathway to nitrous oxide. The broad range of energy-yielding metabolisms possibly explains the ubiquity and high abundance of Woeseiaceae /JTB255 in marine sediments, where they carry out diverse, but yet unknown ecological functions.
Author	Dyksma, Stefan Mußmann, Marc Pjevac, Petra Krüger, Karen
Author_xml	– sequence: 1 givenname: Marc surname: Mußmann fullname: Mußmann, Marc email: mussmann@microbial-ecology.net organization: Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna – sequence: 2 givenname: Petra surname: Pjevac fullname: Pjevac, Petra organization: Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna – sequence: 3 givenname: Karen surname: Krüger fullname: Krüger, Karen organization: Department of Molecular Ecology, Max Planck Institute for Marine Microbiology – sequence: 4 givenname: Stefan surname: Dyksma fullname: Dyksma, Stefan organization: Department of Molecular Ecology, Max Planck Institute for Marine Microbiology
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/28060363$$D View this record in MEDLINE/PubMed
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References	Amaral-ZettlerLArtigasLFBarossJBharathiPALBoetiusAChandramohanDLife in the World’s Oceans2010Wiley-Blackwell22124510.1002/9781444325508.ch12 LiuJLiuXWangMQiaoYZhengYZhangX-HBacterial and archaeal communities in sediments of the North Chinese marginal seasMicrob Ecol2015701051171:CAS:528:DC%2BC2cXitV2gtLfJ10.1007/s00248-014-0553-8 PruesseEQuastEKnittelKFuchsBMLudwigWPepliesJSILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARBNucleic Acids Res200735718871961:CAS:528:DC%2BD1cXhtFGmtg%3D%3D10.1093/nar/gkm864 Marchant HK, Tegetmayer HE, Ahmerkamp S, Holtappels M, Lavik G, Graf J et al. Metabolic specialization of denitrifiers in permeable sediments leads to N2O emissions (under review). BakerBJLazarCSTeskeAPDickGJGenomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteriaMicrobiome201531410.1186/s40168-015-0077-6 BurdigeDJPreservation of organic matter in marine sediments: controls, mechanisms, and an imbalance in sediment organic carbon budgets?Chem Rev20071074674851:CAS:528:DC%2BD2sXot1WmtQ%3D%3D10.1021/cr050347q BowmanJPMcCammonSADannALBiogeographic and quantitative analyses of abundant uncultivated γ-proteobacterial clades from marine sedimentMicrob Ecol2005494514601:STN:280:DC%2BD2MzmslWgtQ%3D%3D10.1007/s00248-004-0070-2 DyksmaSBischofKFuchsBMHoffmannKMeierDMeyerdierksAUbiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sedimentsISME J201610193919531:CAS:528:DC%2BC28Xht12ls7fP10.1038/ismej.2015.257 SorekRZhuYCreeveyCJFrancinoMPBorkPRubinEMGenome-wide experimental determination of barriers to horizontal gene transferScience2007318144914521:CAS:528:DC%2BD2sXhtlGmtLnE10.1126/science.1147112 DuZ-JWangZ-JZhaoJ-XChenG-JWoeseia oceani gen. nov., sp. nov., a chemoheterotrophic member of the order Chromatiales, and proposal of Woeseiaceae fam. novInt J Syst Evol Microbiol2016661071121:CAS:528:DC%2BC28XksF2htrw%3D10.1099/ijsem.0.000683 SchauerRBienholdCRametteAHarderJBacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic OceanISME J201041591701:CAS:528:DC%2BC3cXntVajtA%3D%3D10.1038/ismej.2009.106 RuffSEProbandtDZinkannACIversenMHKlaasCWürzbergLIndications for algae-degrading benthic microbial communities in deep-sea sediments along the Antarctic Polar FrontDeep Sea Res PT II201410861610.1016/j.dsr2.2014.05.011 OrcuttBNSylvanJBKnabNJEdwardsKJMicrobial ecology of the dark ocean above, at, and below the seafloorMicrobiol Mol Biol Rev2011753614221:CAS:528:DC%2BC3MXpslOit7w%3D10.1128/MMBR.00039-10 YarzaPYilmazPPruesseEGloecknerFOLudwigWSchleiferK-HUniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequencesNat Rev Microbiol2014126356451:CAS:528:DC%2BC2cXhtlGnt7vI10.1038/nrmicro3330 ZingerLAmaral-ZettlerLAFuhrmanJAHorner-DevineMCHuseSMWelchDBMGlobal patterns of bacterial beta-diversity in seafloor and seawater ecosystemsPLoS One20116e245701:CAS:528:DC%2BC3MXht1ChsLrM10.1371/journal.pone.0024570 BienholdCZingerLBoetiusARametteADiversity and biogeography of bathyal and abyssal seafloor bacteriaPloS One201611e014801610.1371/journal.pone.0148016 TullyBJHeidelbergJFMicrobial communities associated with ferromanganese nodules and the surrounding sedimentsFront Microbiol2013416110.3389/fmicb.2013.00161 QuastCPruesseEYilmazPGerkenJSchweerTYarzaPThe SILVA ribosomal RNA gene database project: improved data processing and web-based toolsNucleic Acids Res201341D590D5961:CAS:528:DC%2BC38XhvV2ksb%2FN10.1093/nar/gks1219 Fernández-GómezBRichterMSchülerMPinhassiJAcinasSGGonzálezJMEcology of marine Bacteroidetes: a comparative genomics approachISME J201371026103710.1038/ismej.2012.169 GrafDRJonesCMHallinSIntergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissionsPloS One20149e11411810.1371/journal.pone.0114118 Schauer (2024011818562672400_CR16) 2010; 4 2024011818562672400_CR11 Pruesse (2024011818562672400_CR13) 2007; 35 Sorek (2024011818562672400_CR17) 2007; 318 Amaral-Zettler (2024011818562672400_CR1) 2010 Bienhold (2024011818562672400_CR3) 2016; 11 Bowman (2024011818562672400_CR4) 2005; 49 Graf (2024011818562672400_CR9) 2014; 9 Quast (2024011818562672400_CR14) 2013; 41 Du (2024011818562672400_CR6) 2016; 66 Tully (2024011818562672400_CR18) 2013; 4 Baker (2024011818562672400_CR2) 2015; 3 Liu (2024011818562672400_CR10) 2015; 70 Orcutt (2024011818562672400_CR12) 2011; 75 Dyksma (2024011818562672400_CR7) 2016; 10 Fernández-Gómez (2024011818562672400_CR8) 2013; 7 Zinger (2024011818562672400_CR20) 2011; 6 Burdige (2024011818562672400_CR5) 2007; 107 Yarza (2024011818562672400_CR19) 2014; 12 Ruff (2024011818562672400_CR15) 2014; 108
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surface sediments of the South Atlantic Ocean publication-title: ISME J doi: 10.1038/ismej.2009.106 – volume: 6 start-page: e24570 year: 2011 ident: 2024011818562672400_CR20 article-title: Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems publication-title: PLoS One doi: 10.1371/journal.pone.0024570 – volume: 3 start-page: 14 year: 2015 ident: 2024011818562672400_CR2 article-title: Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria publication-title: Microbiome doi: 10.1186/s40168-015-0077-6 – volume: 11 start-page: e0148016 year: 2016 ident: 2024011818562672400_CR3 article-title: Diversity and biogeography of bathyal and abyssal seafloor bacteria publication-title: PloS One doi: 10.1371/journal.pone.0148016 – volume: 318 start-page: 1449 year: 2007 ident: 2024011818562672400_CR17 article-title: Genome-wide experimental determination of barriers to horizontal gene transfer publication-title: Science doi: 10.1126/science.1147112 – volume: 75 start-page: 361 year: 2011 ident: 2024011818562672400_CR12 article-title: Microbial ecology of the dark ocean above, at, and below the seafloor publication-title: Microbiol Mol Biol Rev doi: 10.1128/MMBR.00039-10 – start-page: 221 volume-title: Life in the World’s Oceans year: 2010 ident: 2024011818562672400_CR1 doi: 10.1002/9781444325508.ch12 – volume: 107 start-page: 467 year: 2007 ident: 2024011818562672400_CR5 article-title: Preservation of organic matter in marine sediments: controls, mechanisms, and an imbalance in sediment organic carbon budgets? publication-title: Chem Rev doi: 10.1021/cr050347q – volume: 12 start-page: 635 year: 2014 ident: 2024011818562672400_CR19 article-title: Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences publication-title: Nat Rev Microbiol doi: 10.1038/nrmicro3330
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Snippet	To date, very little is known about the bacterial core community of marine sediments. Here we study the environmental distribution, abundance and ecogenomics...
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SubjectTerms	14/32 14/63 45/23 631/326/171/1878 704/158/855 Australia Autotrophic Processes Biomedical and Life Sciences Ecological function Ecology Evolutionary Biology Gammaproteobacteria - classification Gammaproteobacteria - genetics Gammaproteobacteria - isolation & purification Gammaproteobacteria - metabolism Genome, Bacterial Geologic Sediments - microbiology Heterotrophic Processes Life Sciences Marine sediments Metagenomics Microbial activity Microbial Ecology Microbial Genetics and Genomics Microbiology Nitrous oxide Oceans and Seas Phylogeny RNA, Ribosomal, 16S - genetics Short Communication
Title	Genomic repertoire of the Woeseiaceae/JTB255, cosmopolitan and abundant core members of microbial communities in marine sediments
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