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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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.
Format: Article in Journal/Newspaper
Language:unknown
Published: figshare 2021
Subjects:
Online Access:https://dx.doi.org/10.6084/m9.figshare.c.5668006
https://springernature.figshare.com/collections/Active_virus-host_interactions_at_sub-freezing_temperatures_in_Arctic_peat_soil/5668006
id ftdatacite:10.6084/m9.figshare.c.5668006
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.5668006 2023-05-15T14:58:03+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. 2021 https://dx.doi.org/10.6084/m9.figshare.c.5668006 https://springernature.figshare.com/collections/Active_virus-host_interactions_at_sub-freezing_temperatures_in_Arctic_peat_soil/5668006 unknown figshare https://dx.doi.org/10.1186/s40168-021-01154-2 Creative Commons Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/legalcode cc-by-4.0 CC-BY Microbiology FOS Biological sciences Collection article 2021 ftdatacite https://doi.org/10.6084/m9.figshare.c.5668006 https://doi.org/10.1186/s40168-021-01154-2 2021-11-05T12:55:41Z 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 H218O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO2) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up 18O in soil and respired CO2 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. Video abstract Article in Journal/Newspaper Arctic Alaska DataCite Metadata Store (German National Library of Science and Technology) Arctic Bonanza ENVELOPE(-119.820,-119.820,55.917,55.917)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Microbiology
FOS Biological sciences
spellingShingle Microbiology
FOS Biological sciences
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
FOS Biological sciences
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 H218O or natural abundance water for 184 and 370 days. We sequenced 23 SIP-metagenomes and measured carbon dioxide (CO2) efflux throughout the experiment. We identified 46 bacterial populations (spanning 9 phyla) and 243 viral populations that actively took up 18O in soil and respired CO2 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. Video abstract
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 figshare
publishDate 2021
url https://dx.doi.org/10.6084/m9.figshare.c.5668006
https://springernature.figshare.com/collections/Active_virus-host_interactions_at_sub-freezing_temperatures_in_Arctic_peat_soil/5668006
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_relation https://dx.doi.org/10.1186/s40168-021-01154-2
op_rights Creative Commons Attribution 4.0 International
https://creativecommons.org/licenses/by/4.0/legalcode
cc-by-4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.5668006
https://doi.org/10.1186/s40168-021-01154-2
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