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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Published in:Frontiers in Microbiology
Main Authors: Adrien Vigneron, Connie Lovejoy, Perrine Cruaud, Dimitri Kalenitchenko, Alexander Culley, Warwick F. Vincent
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2019
Subjects:
Ice
Online Access:https://doi.org/10.3389/fmicb.2019.01656
https://doaj.org/article/4fe34c0ea5a8476b862b113c642206cc
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spelling ftdoajarticles:oai:doaj.org/article:4fe34c0ea5a8476b862b113c642206cc 2023-05-15T16:37:06+02:00 Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake Adrien Vigneron Connie Lovejoy Perrine Cruaud Dimitri Kalenitchenko Alexander Culley Warwick F. Vincent 2019-07-01T00:00:00Z https://doi.org/10.3389/fmicb.2019.01656 https://doaj.org/article/4fe34c0ea5a8476b862b113c642206cc EN eng Frontiers Media S.A. https://www.frontiersin.org/article/10.3389/fmicb.2019.01656/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2019.01656 https://doaj.org/article/4fe34c0ea5a8476b862b113c642206cc Frontiers in Microbiology, Vol 10 (2019) MAGs microbial diversity metagenomes methane permafrost thermokarst Microbiology QR1-502 article 2019 ftdoajarticles https://doi.org/10.3389/fmicb.2019.01656 2022-12-31T14:19:59Z 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. Article in Journal/Newspaper Ice permafrost Subarctic Thermokarst Directory of Open Access Journals: DOAJ Articles Frontiers in Microbiology 10
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic MAGs
microbial diversity
metagenomes
methane
permafrost
thermokarst
Microbiology
QR1-502
spellingShingle MAGs
microbial diversity
metagenomes
methane
permafrost
thermokarst
Microbiology
QR1-502
Adrien Vigneron
Connie Lovejoy
Perrine Cruaud
Dimitri Kalenitchenko
Alexander Culley
Warwick F. Vincent
Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake
topic_facet MAGs
microbial diversity
metagenomes
methane
permafrost
thermokarst
Microbiology
QR1-502
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.
format Article in Journal/Newspaper
author Adrien Vigneron
Connie Lovejoy
Perrine Cruaud
Dimitri Kalenitchenko
Alexander Culley
Warwick F. Vincent
author_facet Adrien Vigneron
Connie Lovejoy
Perrine Cruaud
Dimitri Kalenitchenko
Alexander Culley
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.
publishDate 2019
url https://doi.org/10.3389/fmicb.2019.01656
https://doaj.org/article/4fe34c0ea5a8476b862b113c642206cc
genre Ice
permafrost
Subarctic
Thermokarst
genre_facet Ice
permafrost
Subarctic
Thermokarst
op_source Frontiers in Microbiology, Vol 10 (2019)
op_relation https://www.frontiersin.org/article/10.3389/fmicb.2019.01656/full
https://doaj.org/toc/1664-302X
1664-302X
doi:10.3389/fmicb.2019.01656
https://doaj.org/article/4fe34c0ea5a8476b862b113c642206cc
op_doi https://doi.org/10.3389/fmicb.2019.01656
container_title Frontiers in Microbiology
container_volume 10
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