Active virus-host interactions at sub-freezing temperatures in Arctic peat soil

Abstract Background Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake and is primarily driven by microbial decomposers. Viruses modulate microbial carbon cycling via induced mortality and metabolic controls, but it is unknown whether v...

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Published in:Microbiome
Main Authors: Trubl, Gareth, Kimbrel, Jeffrey A., Liquet-Gonzalez, Jose, Nuccio, Erin E., Weber, Peter K., Pett-Ridge, Jennifer, Jansson, Janet K., Waldrop, Mark P., Blazewicz, Steven J.
Other Authors: Lawrence Livermore National Laboratory, Office of Science, National Science Foundation, Pacific Northwest Research Station
Format: Article in Journal/Newspaper
Language:English
Published: Springer Science and Business Media LLC 2021
Subjects:
Online Access:http://dx.doi.org/10.1186/s40168-021-01154-2
https://link.springer.com/content/pdf/10.1186/s40168-021-01154-2.pdf
https://link.springer.com/article/10.1186/s40168-021-01154-2/fulltext.html
id crspringernat:10.1186/s40168-021-01154-2
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spelling crspringernat:10.1186/s40168-021-01154-2 2023-05-15T14:58:14+02:00 Active virus-host interactions at sub-freezing temperatures in Arctic peat soil Trubl, Gareth Kimbrel, Jeffrey A. Liquet-Gonzalez, Jose Nuccio, Erin E. Weber, Peter K. Pett-Ridge, Jennifer Jansson, Janet K. Waldrop, Mark P. Blazewicz, Steven J. Lawrence Livermore National Laboratory Office of Science National Science Foundation Pacific Northwest Research Station 2021 http://dx.doi.org/10.1186/s40168-021-01154-2 https://link.springer.com/content/pdf/10.1186/s40168-021-01154-2.pdf https://link.springer.com/article/10.1186/s40168-021-01154-2/fulltext.html en eng Springer Science and Business Media LLC https://creativecommons.org/licenses/by/4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Microbiome volume 9, issue 1 ISSN 2049-2618 Microbiology (medical) Microbiology journal-article 2021 crspringernat https://doi.org/10.1186/s40168-021-01154-2 2022-01-04T07:28:05Z Abstract Background Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake and is primarily driven by microbial decomposers. Viruses modulate microbial carbon cycling via induced mortality and metabolic controls, but it is unknown whether viruses are active under winter conditions (anoxic and sub-freezing temperatures). Results We used stable isotope probing (SIP) targeted metagenomics to reveal the genomic potential of active soil microbial populations under simulated winter conditions, with an emphasis on viruses and virus-host dynamics. Arctic peat soils from the Bonanza Creek Long-Term Ecological Research site in Alaska were incubated under sub-freezing anoxic conditions with H 2 18 O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO 2 ) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up 18 O in soil and respired CO 2 throughout the incubation. Active bacterial populations represented only a small portion of the detected microbial community and were capable of fermentation and organic matter degradation. In contrast, active viral populations represented a large portion of the detected viral community and one third were linked to active bacterial populations. We identified 86 auxiliary metabolic genes and other environmentally relevant genes. The majority of these genes were carried by active viral populations and had diverse functions such as carbon utilization and scavenging that could provide their host with a fitness advantage for utilizing much-needed carbon sources or acquiring essential nutrients. Conclusions Overall, there was a stark difference in the identity and function of the active bacterial and viral community compared to the unlabeled community that would have been overlooked with a non-targeted standard metagenomic analysis. Our results illustrate that substantial active virus-host interactions occur in sub-freezing anoxic conditions and highlight viruses as a major community-structuring agent that likely modulates carbon loss in peat soils during winter, which may be pivotal for understanding the future fate of arctic soils' vast carbon stocks. Article in Journal/Newspaper Arctic Alaska Springer Nature (via Crossref) Arctic Bonanza ENVELOPE(-119.820,-119.820,55.917,55.917) Microbiome 9 1
institution Open Polar
collection Springer Nature (via Crossref)
op_collection_id crspringernat
language English
topic Microbiology (medical)
Microbiology
spellingShingle Microbiology (medical)
Microbiology
Trubl, Gareth
Kimbrel, Jeffrey A.
Liquet-Gonzalez, Jose
Nuccio, Erin E.
Weber, Peter K.
Pett-Ridge, Jennifer
Jansson, Janet K.
Waldrop, Mark P.
Blazewicz, Steven J.
Active virus-host interactions at sub-freezing temperatures in Arctic peat soil
topic_facet Microbiology (medical)
Microbiology
description Abstract Background Winter carbon loss in northern ecosystems is estimated to be greater than the average growing season carbon uptake and is primarily driven by microbial decomposers. Viruses modulate microbial carbon cycling via induced mortality and metabolic controls, but it is unknown whether viruses are active under winter conditions (anoxic and sub-freezing temperatures). Results We used stable isotope probing (SIP) targeted metagenomics to reveal the genomic potential of active soil microbial populations under simulated winter conditions, with an emphasis on viruses and virus-host dynamics. Arctic peat soils from the Bonanza Creek Long-Term Ecological Research site in Alaska were incubated under sub-freezing anoxic conditions with H 2 18 O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO 2 ) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up 18 O in soil and respired CO 2 throughout the incubation. Active bacterial populations represented only a small portion of the detected microbial community and were capable of fermentation and organic matter degradation. In contrast, active viral populations represented a large portion of the detected viral community and one third were linked to active bacterial populations. We identified 86 auxiliary metabolic genes and other environmentally relevant genes. The majority of these genes were carried by active viral populations and had diverse functions such as carbon utilization and scavenging that could provide their host with a fitness advantage for utilizing much-needed carbon sources or acquiring essential nutrients. Conclusions Overall, there was a stark difference in the identity and function of the active bacterial and viral community compared to the unlabeled community that would have been overlooked with a non-targeted standard metagenomic analysis. Our results illustrate that substantial active virus-host interactions occur in sub-freezing anoxic conditions and highlight viruses as a major community-structuring agent that likely modulates carbon loss in peat soils during winter, which may be pivotal for understanding the future fate of arctic soils' vast carbon stocks.
author2 Lawrence Livermore National Laboratory
Office of Science
National Science Foundation
Pacific Northwest Research Station
format Article in Journal/Newspaper
author Trubl, Gareth
Kimbrel, Jeffrey A.
Liquet-Gonzalez, Jose
Nuccio, Erin E.
Weber, Peter K.
Pett-Ridge, Jennifer
Jansson, Janet K.
Waldrop, Mark P.
Blazewicz, Steven J.
author_facet Trubl, Gareth
Kimbrel, Jeffrey A.
Liquet-Gonzalez, Jose
Nuccio, Erin E.
Weber, Peter K.
Pett-Ridge, Jennifer
Jansson, Janet K.
Waldrop, Mark P.
Blazewicz, Steven J.
author_sort Trubl, Gareth
title Active virus-host interactions at sub-freezing temperatures in Arctic peat soil
title_short Active virus-host interactions at sub-freezing temperatures in Arctic peat soil
title_full Active virus-host interactions at sub-freezing temperatures in Arctic peat soil
title_fullStr Active virus-host interactions at sub-freezing temperatures in Arctic peat soil
title_full_unstemmed Active virus-host interactions at sub-freezing temperatures in Arctic peat soil
title_sort active virus-host interactions at sub-freezing temperatures in arctic peat soil
publisher Springer Science and Business Media LLC
publishDate 2021
url http://dx.doi.org/10.1186/s40168-021-01154-2
https://link.springer.com/content/pdf/10.1186/s40168-021-01154-2.pdf
https://link.springer.com/article/10.1186/s40168-021-01154-2/fulltext.html
long_lat ENVELOPE(-119.820,-119.820,55.917,55.917)
geographic Arctic
Bonanza
geographic_facet Arctic
Bonanza
genre Arctic
Alaska
genre_facet Arctic
Alaska
op_source Microbiome
volume 9, issue 1
ISSN 2049-2618
op_rights https://creativecommons.org/licenses/by/4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.1186/s40168-021-01154-2
container_title Microbiome
container_volume 9
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