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

Microbiome

Research

Zhi-Ping Zhong¹  Matthew B. Sullivan²  Josephine Z. Rapp³  Olivier Zablocki⁴  Dean Vik⁴  Heather Maughan⁵  Ben Temperton⁶  Jody W. Deming⁷ 

[1] Byrd Polar and Climate Research Center, Ohio State University, Columbus, OH, USA;Department of Microbiology, Ohio State University, Columbus, OH, USA;Center of Microbiome Science, Ohio State University, Columbus, OH, USA;Byrd Polar and Climate Research Center, Ohio State University, Columbus, OH, USA;Department of Microbiology, Ohio State University, Columbus, OH, USA;Center of Microbiome Science, Ohio State University, Columbus, OH, USA;Department of Civil, Environmental and Geodetic Engineering, Ohio State University, Columbus, OH, USA;Department of Biology, Université Laval, Québec, QC, Canada;Center for Northern Studies (CEN), Université Laval, Québec, QC, Canada;Department of Microbiology, Ohio State University, Columbus, OH, USA;Center of Microbiome Science, Ohio State University, Columbus, OH, USA;Ronin Institute, Montclair, NJ, USA;School of Biosciences, University of Exeter, Exeter, Devon, UK;School of Oceanography and Astrobiology Program, University of Washington, Seattle, WA, USA;

关键词: Arctic;    Viruses;    Subzero and hypersaline brines;    Cryopeg brine;    Sea ice brine;    Long- and short-read viromics;    Metatranscriptomics;    Population genetics;    Evolution;    Gene transfer;   

DOI  :  10.1186/s40168-023-01619-6

 received in 2023-01-12, accepted in 2023-07-12,  发布年份 2023

来源: Springer

【 摘 要 】

BackgroundClimate 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.ResultsWe 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.ConclusionsOur results confirmed the benefits of long-read-powered viromics in understanding the environmental virosphere through significantly improved genomic recovery, expanding viral discovery and the potential for biological inference. Evidence of viruses actively infecting the dominant microbes in subzero brines and modulating host metabolism underscored the potential impact of viruses on these remote and underexplored extreme ecosystems. Microdiversity results shed light on different strategies viruses use to evolve and adapt when extreme conditions are stable versus fluctuating. Together, these findings verify the value of long-read-powered viromics and provide foundational data on viral evolution and virus-microbe interactions in Earth’s destabilized and rapidly disappearing cryosphere.B3KUN5MJ8EAz4vqucsgZtLVideo Abstract

【 授权许可】

CC BY   
© BioMed Central Ltd., part of Springer Nature 2023

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