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

Abstract

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 activemore » 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.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1826202
Alternate Identifier(s):
OSTI ID: 1830222
Report Number(s):
PNNL-SA-162885
Journal ID: ISSN 2049-2618; 208; PII: 1154
Grant/Contract Number:  
18-ERD-041; SCW1632; AC05-76RL01830
Resource Type:
Published Article
Journal Name:
Microbiome
Additional Journal Information:
Journal Name: Microbiome Journal Volume: 9 Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English
Subject:
soil viruses, bacteriophage, stable isotope probing, permafrost, peat, o-water, metagenomics

Citation Formats

Trubl, Gareth, Kimbrel, Jeffrey A., Liquet-Gonzalez, Jose, Nuccio, Erin E., Weber, Peter K., Pett-Ridge, Jennifer, Jansson, Janet K., Waldrop, Mark P., and Blazewicz, Steven J.. Active virus-host interactions at sub-freezing temperatures in Arctic peat soil. United Kingdom: N. p., 2021. Web. https://doi.org/10.1186/s40168-021-01154-2.
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. United Kingdom. https://doi.org/10.1186/s40168-021-01154-2
Trubl, Gareth, Kimbrel, Jeffrey A., Liquet-Gonzalez, Jose, Nuccio, Erin E., Weber, Peter K., Pett-Ridge, Jennifer, Jansson, Janet K., Waldrop, Mark P., and Blazewicz, Steven J.. Mon . "Active virus-host interactions at sub-freezing temperatures in Arctic peat soil". United Kingdom. https://doi.org/10.1186/s40168-021-01154-2.
@article{osti_1826202,
title = {Active virus-host interactions at sub-freezing temperatures in Arctic peat soil},
author = {Trubl, Gareth and Kimbrel, Jeffrey A. and Liquet-Gonzalez, Jose and Nuccio, Erin E. and Weber, Peter K. and Pett-Ridge, Jennifer and Jansson, Janet K. and Waldrop, Mark P. and Blazewicz, Steven J.},
abstractNote = {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.},
doi = {10.1186/s40168-021-01154-2},
journal = {Microbiome},
number = 1,
volume = 9,
place = {United Kingdom},
year = {2021},
month = {10}
}

Journal Article:
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https://doi.org/10.1186/s40168-021-01154-2

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