Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice

ABSTRACT Arctic regions, which are changing rapidly as they warm 2 to 3 times faster than the global average, still retain microbial habitats that serve as natural laboratories for understanding mechanisms of microbial adaptation to extreme conditions. Seawater-derived brines within both sea ice (se...

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Published in:mSystems
Main Authors: Zhi-Ping Zhong, Josephine Z. Rapp, James M. Wainaina, Natalie E. Solonenko, Heather Maughan, Shelly D. Carpenter, Zachary S. Cooper, Ho Bin Jang, Benjamin Bolduc, Jody W. Deming, Matthew B. Sullivan
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2020
Subjects:
Ice
Online Access:https://doi.org/10.1128/mSystems.00246-20
https://doaj.org/article/9d37cf666bdd4ac4aac9aa1544dfaf41
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spelling ftdoajarticles:oai:doaj.org/article:9d37cf666bdd4ac4aac9aa1544dfaf41 2023-05-15T14:56:51+02:00 Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice Zhi-Ping Zhong Josephine Z. Rapp James M. Wainaina Natalie E. Solonenko Heather Maughan Shelly D. Carpenter Zachary S. Cooper Ho Bin Jang Benjamin Bolduc Jody W. Deming Matthew B. Sullivan 2020-06-01T00:00:00Z https://doi.org/10.1128/mSystems.00246-20 https://doaj.org/article/9d37cf666bdd4ac4aac9aa1544dfaf41 EN eng American Society for Microbiology https://journals.asm.org/doi/10.1128/mSystems.00246-20 https://doaj.org/toc/2379-5077 doi:10.1128/mSystems.00246-20 2379-5077 https://doaj.org/article/9d37cf666bdd4ac4aac9aa1544dfaf41 mSystems, Vol 5, Iss 3 (2020) viral communities extreme environments virus-host interaction cold and salt adaption horizontal gene transfer Microbiology QR1-502 article 2020 ftdoajarticles https://doi.org/10.1128/mSystems.00246-20 2022-12-31T13:54:27Z ABSTRACT Arctic regions, which are changing rapidly as they warm 2 to 3 times faster than the global average, still retain microbial habitats that serve as natural laboratories for understanding mechanisms of microbial adaptation to extreme conditions. Seawater-derived brines within both sea ice (sea-ice brine) and ancient layers of permafrost (cryopeg brine) support diverse microbes adapted to subzero temperatures and high salinities, yet little is known about viruses in these extreme environments, which, if analogous to other systems, could play important evolutionary and ecosystem roles. Here, we characterized viral communities and their functions in samples of cryopeg brine, sea-ice brine, and melted sea ice. Viral abundance was high in cryopeg brine (1.2 × 108 ml−1) and much lower in sea-ice brine (1.3 × 105 to 2.1 × 105 ml−1), which roughly paralleled the differences in cell concentrations in these samples. Five low-input, quantitative viral metagenomes were sequenced to yield 476 viral populations (i.e., species level; ≥10 kb), only 12% of which could be assigned taxonomy by traditional database approaches, indicating a high degree of novelty. Additional analyses revealed that these viruses: (i) formed communities that differed between sample type and vertically with sea-ice depth; (ii) infected hosts that dominated these extreme ecosystems, including Marinobacter, Glaciecola, and Colwellia; and (iii) encoded fatty acid desaturase (FAD) genes that likely helped their hosts overcome cold and salt stress during infection, as well as mediated horizontal gene transfer of FAD genes between microbes. Together, these findings contribute to understanding viral abundances and communities and how viruses impact their microbial hosts in subzero brines and sea ice. IMPORTANCE This study explores viral community structure and function in remote and extreme Arctic environments, including subzero brines within marine layers of permafrost and sea ice, using a modern viral ecogenomics toolkit for the first time. In ... Article in Journal/Newspaper Arctic Ice permafrost Sea ice Directory of Open Access Journals: DOAJ Articles Arctic mSystems 5 3
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic viral communities
extreme environments
virus-host interaction
cold and salt adaption
horizontal gene transfer
Microbiology
QR1-502
spellingShingle viral communities
extreme environments
virus-host interaction
cold and salt adaption
horizontal gene transfer
Microbiology
QR1-502
Zhi-Ping Zhong
Josephine Z. Rapp
James M. Wainaina
Natalie E. Solonenko
Heather Maughan
Shelly D. Carpenter
Zachary S. Cooper
Ho Bin Jang
Benjamin Bolduc
Jody W. Deming
Matthew B. Sullivan
Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice
topic_facet viral communities
extreme environments
virus-host interaction
cold and salt adaption
horizontal gene transfer
Microbiology
QR1-502
description ABSTRACT Arctic regions, which are changing rapidly as they warm 2 to 3 times faster than the global average, still retain microbial habitats that serve as natural laboratories for understanding mechanisms of microbial adaptation to extreme conditions. Seawater-derived brines within both sea ice (sea-ice brine) and ancient layers of permafrost (cryopeg brine) support diverse microbes adapted to subzero temperatures and high salinities, yet little is known about viruses in these extreme environments, which, if analogous to other systems, could play important evolutionary and ecosystem roles. Here, we characterized viral communities and their functions in samples of cryopeg brine, sea-ice brine, and melted sea ice. Viral abundance was high in cryopeg brine (1.2 × 108 ml−1) and much lower in sea-ice brine (1.3 × 105 to 2.1 × 105 ml−1), which roughly paralleled the differences in cell concentrations in these samples. Five low-input, quantitative viral metagenomes were sequenced to yield 476 viral populations (i.e., species level; ≥10 kb), only 12% of which could be assigned taxonomy by traditional database approaches, indicating a high degree of novelty. Additional analyses revealed that these viruses: (i) formed communities that differed between sample type and vertically with sea-ice depth; (ii) infected hosts that dominated these extreme ecosystems, including Marinobacter, Glaciecola, and Colwellia; and (iii) encoded fatty acid desaturase (FAD) genes that likely helped their hosts overcome cold and salt stress during infection, as well as mediated horizontal gene transfer of FAD genes between microbes. Together, these findings contribute to understanding viral abundances and communities and how viruses impact their microbial hosts in subzero brines and sea ice. IMPORTANCE This study explores viral community structure and function in remote and extreme Arctic environments, including subzero brines within marine layers of permafrost and sea ice, using a modern viral ecogenomics toolkit for the first time. In ...
format Article in Journal/Newspaper
author Zhi-Ping Zhong
Josephine Z. Rapp
James M. Wainaina
Natalie E. Solonenko
Heather Maughan
Shelly D. Carpenter
Zachary S. Cooper
Ho Bin Jang
Benjamin Bolduc
Jody W. Deming
Matthew B. Sullivan
author_facet Zhi-Ping Zhong
Josephine Z. Rapp
James M. Wainaina
Natalie E. Solonenko
Heather Maughan
Shelly D. Carpenter
Zachary S. Cooper
Ho Bin Jang
Benjamin Bolduc
Jody W. Deming
Matthew B. Sullivan
author_sort Zhi-Ping Zhong
title Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice
title_short Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice
title_full Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice
title_fullStr Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice
title_full_unstemmed Viral Ecogenomics of Arctic Cryopeg Brine and Sea Ice
title_sort viral ecogenomics of arctic cryopeg brine and sea ice
publisher American Society for Microbiology
publishDate 2020
url https://doi.org/10.1128/mSystems.00246-20
https://doaj.org/article/9d37cf666bdd4ac4aac9aa1544dfaf41
geographic Arctic
geographic_facet Arctic
genre Arctic
Ice
permafrost
Sea ice
genre_facet Arctic
Ice
permafrost
Sea ice
op_source mSystems, Vol 5, Iss 3 (2020)
op_relation https://journals.asm.org/doi/10.1128/mSystems.00246-20
https://doaj.org/toc/2379-5077
doi:10.1128/mSystems.00246-20
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https://doaj.org/article/9d37cf666bdd4ac4aac9aa1544dfaf41
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