Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines

BACKGROUND: Climate change threatens Earth’s ice-based ecosystems which currently offer archives and eco-evolutionary experiments in the extreme. Arctic cryopeg brine (marine-derived, within permafrost) and sea ice brine, similar in subzero temperature and high salinity but different in temporal sta...

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Published in:Microbiome
Main Authors: Zhong, Zhi-Ping, Vik, Dean, Rapp, Josephine Z., Zablocki, Olivier, Maughan, Heather, Temperton, Ben, Deming, Jody W., Sullivan, Matthew B.
Format: Text
Language:English
Published: BioMed Central 2023
Subjects:
Ice
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405475/
http://www.ncbi.nlm.nih.gov/pubmed/37550784
https://doi.org/10.1186/s40168-023-01619-6
id ftpubmed:oai:pubmedcentral.nih.gov:10405475
record_format openpolar
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research
spellingShingle Research
Zhong, Zhi-Ping
Vik, Dean
Rapp, Josephine Z.
Zablocki, Olivier
Maughan, Heather
Temperton, Ben
Deming, Jody W.
Sullivan, Matthew B.
Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines
topic_facet Research
description BACKGROUND: Climate change threatens Earth’s ice-based ecosystems which currently offer archives and eco-evolutionary experiments in the extreme. Arctic cryopeg brine (marine-derived, within permafrost) and sea ice brine, similar in subzero temperature and high salinity but different in temporal stability, are inhabited by microbes adapted to these extreme conditions. However, little is known about their viruses (community composition, diversity, interaction with hosts, or evolution) or how they might respond to geologically stable cryopeg versus fluctuating sea ice conditions. RESULTS: We used long- and short-read viromics and metatranscriptomics to study viruses in Arctic cryopeg brine, sea ice brine, and underlying seawater, recovering 11,088 vOTUs (~species-level taxonomic unit), a 4.4-fold increase of known viruses in these brines. More specifically, the long-read-powered viromes doubled the number of longer (≥25 kb) vOTUs generated and recovered more hypervariable regions by >5-fold compared to short-read viromes. Distribution assessment, by comparing to known viruses in public databases, supported that cryopeg brine viruses were of marine origin yet distinct from either sea ice brine or seawater viruses, while 94% of sea ice brine viruses were also present in seawater. A virus-encoded, ecologically important exopolysaccharide biosynthesis gene was identified, and many viruses (~half of metatranscriptome-inferred “active” vOTUs) were predicted as actively infecting the dominant microbial genera Marinobacter and Polaribacter in cryopeg and sea ice brines, respectively. Evolutionarily, microdiversity (intra-species genetic variations) analyses suggested that viruses within the stable cryopeg brine were under significantly lower evolutionary pressures than those in the fluctuating sea ice environment, while many sea ice brine virus-tail genes were under positive selection, indicating virus-host co-evolutionary arms races. CONCLUSIONS: Our results confirmed the benefits of long-read-powered viromics in ...
format Text
author Zhong, Zhi-Ping
Vik, Dean
Rapp, Josephine Z.
Zablocki, Olivier
Maughan, Heather
Temperton, Ben
Deming, Jody W.
Sullivan, Matthew B.
author_facet Zhong, Zhi-Ping
Vik, Dean
Rapp, Josephine Z.
Zablocki, Olivier
Maughan, Heather
Temperton, Ben
Deming, Jody W.
Sullivan, Matthew B.
author_sort Zhong, Zhi-Ping
title Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines
title_short Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines
title_full Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines
title_fullStr Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines
title_full_unstemmed Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines
title_sort lower viral evolutionary pressure under stable versus fluctuating conditions in subzero arctic brines
publisher BioMed Central
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405475/
http://www.ncbi.nlm.nih.gov/pubmed/37550784
https://doi.org/10.1186/s40168-023-01619-6
geographic Arctic
geographic_facet Arctic
genre Arctic
Climate change
Ice
permafrost
Sea ice
genre_facet Arctic
Climate change
Ice
permafrost
Sea ice
op_source Microbiome
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405475/
http://www.ncbi.nlm.nih.gov/pubmed/37550784
http://dx.doi.org/10.1186/s40168-023-01619-6
op_rights © BioMed Central Ltd., part of Springer Nature 2023
https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
op_doi https://doi.org/10.1186/s40168-023-01619-6
container_title Microbiome
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10405475 2023-09-05T13:17:06+02:00 Lower viral evolutionary pressure under stable versus fluctuating conditions in subzero Arctic brines Zhong, Zhi-Ping Vik, Dean Rapp, Josephine Z. Zablocki, Olivier Maughan, Heather Temperton, Ben Deming, Jody W. Sullivan, Matthew B. 2023-08-07 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405475/ http://www.ncbi.nlm.nih.gov/pubmed/37550784 https://doi.org/10.1186/s40168-023-01619-6 en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405475/ http://www.ncbi.nlm.nih.gov/pubmed/37550784 http://dx.doi.org/10.1186/s40168-023-01619-6 © BioMed Central Ltd., part of Springer Nature 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Microbiome Research Text 2023 ftpubmed https://doi.org/10.1186/s40168-023-01619-6 2023-08-13T00:52:54Z BACKGROUND: Climate change threatens Earth’s ice-based ecosystems which currently offer archives and eco-evolutionary experiments in the extreme. Arctic cryopeg brine (marine-derived, within permafrost) and sea ice brine, similar in subzero temperature and high salinity but different in temporal stability, are inhabited by microbes adapted to these extreme conditions. However, little is known about their viruses (community composition, diversity, interaction with hosts, or evolution) or how they might respond to geologically stable cryopeg versus fluctuating sea ice conditions. RESULTS: We used long- and short-read viromics and metatranscriptomics to study viruses in Arctic cryopeg brine, sea ice brine, and underlying seawater, recovering 11,088 vOTUs (~species-level taxonomic unit), a 4.4-fold increase of known viruses in these brines. More specifically, the long-read-powered viromes doubled the number of longer (≥25 kb) vOTUs generated and recovered more hypervariable regions by >5-fold compared to short-read viromes. Distribution assessment, by comparing to known viruses in public databases, supported that cryopeg brine viruses were of marine origin yet distinct from either sea ice brine or seawater viruses, while 94% of sea ice brine viruses were also present in seawater. A virus-encoded, ecologically important exopolysaccharide biosynthesis gene was identified, and many viruses (~half of metatranscriptome-inferred “active” vOTUs) were predicted as actively infecting the dominant microbial genera Marinobacter and Polaribacter in cryopeg and sea ice brines, respectively. Evolutionarily, microdiversity (intra-species genetic variations) analyses suggested that viruses within the stable cryopeg brine were under significantly lower evolutionary pressures than those in the fluctuating sea ice environment, while many sea ice brine virus-tail genes were under positive selection, indicating virus-host co-evolutionary arms races. CONCLUSIONS: Our results confirmed the benefits of long-read-powered viromics in ... Text Arctic Climate change Ice permafrost Sea ice PubMed Central (PMC) Arctic Microbiome 11 1