Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake
Permafrost thawing results in the formation of thermokarst lakes, which are biogeochemical hotspots in northern landscapes and strong emitters of greenhouse gasses to the atmosphere. Most studies of thermokarst lakes have been in summer, despite the predominance of winter and ice-cover over much of...
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doaj-4fe34c0ea5a8476b862b113c642206cc2020-11-25T02:22:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-07-011010.3389/fmicb.2019.01656455778Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw LakeAdrien Vigneron0Adrien Vigneron1Adrien Vigneron2Connie Lovejoy3Connie Lovejoy4Connie Lovejoy5Connie Lovejoy6Perrine Cruaud7Perrine Cruaud8Dimitri Kalenitchenko9Dimitri Kalenitchenko10Dimitri Kalenitchenko11Alexander Culley12Alexander Culley13Alexander Culley14Warwick F. Vincent15Warwick F. Vincent16Warwick F. Vincent17Département de Biologie, Université Laval, Quebec, QC, CanadaCentre d’Études Nordiques, Takuvik Joint International Laboratory, Université Laval, Quebec, QC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, CanadaDépartement de Biologie, Université Laval, Quebec, QC, CanadaCentre d’Études Nordiques, Takuvik Joint International Laboratory, Université Laval, Quebec, QC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, CanadaQuébec Océan, Université Laval, Quebec, QC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, CanadaDépartement de Biochimie, de Microbiologie et de Bio-Informatique, Université Laval, Quebec, QC, CanadaDépartement de Biologie, Université Laval, Quebec, QC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, CanadaQuébec Océan, Université Laval, Quebec, QC, CanadaCentre d’Études Nordiques, Takuvik Joint International Laboratory, Université Laval, Quebec, QC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, CanadaDépartement de Biochimie, de Microbiologie et de Bio-Informatique, Université Laval, Quebec, QC, CanadaDépartement de Biologie, Université Laval, Quebec, QC, CanadaCentre d’Études Nordiques, Takuvik Joint International Laboratory, Université Laval, Quebec, QC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, CanadaPermafrost thawing results in the formation of thermokarst lakes, which are biogeochemical hotspots in northern landscapes and strong emitters of greenhouse gasses to the atmosphere. Most studies of thermokarst lakes have been in summer, despite the predominance of winter and ice-cover over much of the year, and the microbial ecology of these waters under ice remains poorly understood. Here we first compared the summer versus winter microbiomes of a subarctic thermokarst lake using DNA- and RNA-based 16S rRNA amplicon sequencing and qPCR. We then applied comparative metagenomics and used genomic bin reconstruction to compare the two seasons for changes in potential metabolic functions in the thermokarst lake microbiome. In summer, the microbial community was dominated by Actinobacteria and Betaproteobacteria, with phototrophic and aerobic pathways consistent with the utilization of labile and photodegraded substrates. The microbial community was strikingly different in winter, with dominance of methanogens, Planctomycetes, Chloroflexi and Deltaproteobacteria, along with various taxa of the Patescibacteria/Candidate Phyla Radiation (Parcubacteria, Microgenomates, Omnitrophica, Aminicenantes). The latter group was underestimated or absent in the amplicon survey, but accounted for about a third of the metagenomic reads. The winter lineages were associated with multiple reductive metabolic processes, fermentations and pathways for the mobilization and degradation of complex organic matter, along with a strong potential for syntrophy or cross-feeding. The results imply that the summer community represents a transient stage of the annual cycle, and that carbon dioxide and methane production continue through the prolonged season of ice cover via a taxonomically distinct winter community and diverse mechanisms of permafrost carbon transformation.https://www.frontiersin.org/article/10.3389/fmicb.2019.01656/fullMAGsmicrobial diversitymetagenomesmethanepermafrostthermokarst |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Adrien Vigneron Adrien Vigneron Adrien Vigneron Connie Lovejoy Connie Lovejoy Connie Lovejoy Connie Lovejoy Perrine Cruaud Perrine Cruaud Dimitri Kalenitchenko Dimitri Kalenitchenko Dimitri Kalenitchenko Alexander Culley Alexander Culley Alexander Culley Warwick F. Vincent Warwick F. Vincent Warwick F. Vincent |
spellingShingle |
Adrien Vigneron Adrien Vigneron Adrien Vigneron Connie Lovejoy Connie Lovejoy Connie Lovejoy Connie Lovejoy Perrine Cruaud Perrine Cruaud Dimitri Kalenitchenko Dimitri Kalenitchenko Dimitri Kalenitchenko Alexander Culley Alexander Culley Alexander Culley Warwick F. Vincent Warwick F. Vincent Warwick F. Vincent Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake Frontiers in Microbiology MAGs microbial diversity metagenomes methane permafrost thermokarst |
author_facet |
Adrien Vigneron Adrien Vigneron Adrien Vigneron Connie Lovejoy Connie Lovejoy Connie Lovejoy Connie Lovejoy Perrine Cruaud Perrine Cruaud Dimitri Kalenitchenko Dimitri Kalenitchenko Dimitri Kalenitchenko Alexander Culley Alexander Culley Alexander Culley Warwick F. Vincent Warwick F. Vincent Warwick F. Vincent |
author_sort |
Adrien Vigneron |
title |
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake |
title_short |
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake |
title_full |
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake |
title_fullStr |
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake |
title_full_unstemmed |
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake |
title_sort |
contrasting winter versus summer microbial communities and metabolic functions in a permafrost thaw lake |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2019-07-01 |
description |
Permafrost thawing results in the formation of thermokarst lakes, which are biogeochemical hotspots in northern landscapes and strong emitters of greenhouse gasses to the atmosphere. Most studies of thermokarst lakes have been in summer, despite the predominance of winter and ice-cover over much of the year, and the microbial ecology of these waters under ice remains poorly understood. Here we first compared the summer versus winter microbiomes of a subarctic thermokarst lake using DNA- and RNA-based 16S rRNA amplicon sequencing and qPCR. We then applied comparative metagenomics and used genomic bin reconstruction to compare the two seasons for changes in potential metabolic functions in the thermokarst lake microbiome. In summer, the microbial community was dominated by Actinobacteria and Betaproteobacteria, with phototrophic and aerobic pathways consistent with the utilization of labile and photodegraded substrates. The microbial community was strikingly different in winter, with dominance of methanogens, Planctomycetes, Chloroflexi and Deltaproteobacteria, along with various taxa of the Patescibacteria/Candidate Phyla Radiation (Parcubacteria, Microgenomates, Omnitrophica, Aminicenantes). The latter group was underestimated or absent in the amplicon survey, but accounted for about a third of the metagenomic reads. The winter lineages were associated with multiple reductive metabolic processes, fermentations and pathways for the mobilization and degradation of complex organic matter, along with a strong potential for syntrophy or cross-feeding. The results imply that the summer community represents a transient stage of the annual cycle, and that carbon dioxide and methane production continue through the prolonged season of ice cover via a taxonomically distinct winter community and diverse mechanisms of permafrost carbon transformation. |
topic |
MAGs microbial diversity metagenomes methane permafrost thermokarst |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2019.01656/full |
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