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Title: Glacier ice archives nearly 15,000-year-old microbes and phages

Abstract

Background Glacier ice archives information, including microbiology, that helps reveal paleoclimate histories and predict future climate change. Though glacier-ice microbes are studied using culture or amplicon approaches, more challenging metagenomic approaches, which provide access to functional, genome-resolved information and viruses, are under-utilized, partly due to low biomass and potential contamination. Results We expand existing clean sampling procedures using controlled artificial ice-core experiments and adapted previously established low-biomass metagenomic approaches to study glacier-ice viruses. Controlled sampling experiments drastically reduced mock contaminants including bacteria, viruses, and free DNA to background levels. Amplicon sequencing from eight depths of two Tibetan Plateau ice cores revealed common glacier-ice lineages including Janthinobacterium, Polaromonas, Herminiimonas, Flavobacterium, Sphingomonas, and Methylobacterium as the dominant genera, while microbial communities were significantly different between two ice cores, associating with different climate conditions during deposition. Separately, ~355- and ~14,400-year-old ice were subject to viral enrichment and low-input quantitative sequencing, yielding genomic sequences for 33 vOTUs. These were virtually all unique to this study, representing 28 novel genera and not a single species shared with 225 environmentally diverse viromes. Further, 42.4% of the vOTUs were identifiable temperate, which is significantly higher than that in gut, soil, and marine viromes, and indicates that temperatemore » phages are possibly favored in glacier-ice environments before being frozen. In silico host predictions linked 18 vOTUs to co-occurring abundant bacteria (Methylobacterium, Sphingomonas, and Janthinobacterium), indicating that these phages infected ice-abundant bacterial groups before being archived. Functional genome annotation revealed four virus-encoded auxiliary metabolic genes, particularly two motility genes suggest viruses potentially facilitate nutrient acquisition for their hosts. Finally, given their possible importance to methane cycling in ice, we focused on Methylobacterium viruses by contextualizing our ice-observed viruses against 123 viromes and prophages extracted from 131 Methylobacterium genomes, revealing that the archived viruses might originate from soil or plants. Conclusions Together, these efforts further microbial and viral sampling procedures for glacier ice and provide a first window into viral communities and functions in ancient glacier environments. Such methods and datasets can potentially enable researchers to contextualize new discoveries and begin to incorporate glacier-ice microbes and their viruses relative to past and present climate change in geographically diverse regions globally.« less

Authors:
ORCiD logo [1];  [1];  [2];  [1];  [1];  [1];  [1];  [3];  [1];  [1];  [1];  [1]
+ Show Author Affiliations
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Univ. of Nebraska, Lincoln, NE (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1813410
Grant/Contract Number:  
AC02-05CH11231; 1502919; 3790
Resource Type:
Accepted Manuscript
Journal Name:
Microbiome
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Guliya ice cap; mountain glacier ice; surface decontamination; ice microbes; ice viruses; Methylobacterium; Sphingomonas; Janthinobacterium

Citation Formats

Zhong, Zhi-Ping, Tian, Funing, Roux, Simon, Gazitúa, M. Consuelo, Solonenko, Natalie E., Li, Yueh-Fen, Davis, Mary E., Van Etten, James L., Mosley-Thompson, Ellen, Rich, Virginia I., Sullivan, Matthew B., and Thompson, Lonnie G. Glacier ice archives nearly 15,000-year-old microbes and phages. United States: N. p., 2021. Web. doi:10.1186/s40168-021-01106-w.
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Zhong, Zhi-Ping, Tian, Funing, Roux, Simon, Gazitúa, M. Consuelo, Solonenko, Natalie E., Li, Yueh-Fen, Davis, Mary E., Van Etten, James L., Mosley-Thompson, Ellen, Rich, Virginia I., Sullivan, Matthew B., & Thompson, Lonnie G. Glacier ice archives nearly 15,000-year-old microbes and phages. United States. https://doi.org/10.1186/s40168-021-01106-w
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Zhong, Zhi-Ping, Tian, Funing, Roux, Simon, Gazitúa, M. Consuelo, Solonenko, Natalie E., Li, Yueh-Fen, Davis, Mary E., Van Etten, James L., Mosley-Thompson, Ellen, Rich, Virginia I., Sullivan, Matthew B., and Thompson, Lonnie G. Tue . "Glacier ice archives nearly 15,000-year-old microbes and phages". United States. https://doi.org/10.1186/s40168-021-01106-w. https://www.osti.gov/servlets/purl/1813410.
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@article{osti_1813410,
title = {Glacier ice archives nearly 15,000-year-old microbes and phages},
author = {Zhong, Zhi-Ping and Tian, Funing and Roux, Simon and Gazitúa, M. Consuelo and Solonenko, Natalie E. and Li, Yueh-Fen and Davis, Mary E. and Van Etten, James L. and Mosley-Thompson, Ellen and Rich, Virginia I. and Sullivan, Matthew B. and Thompson, Lonnie G.},
abstractNote = {Background Glacier ice archives information, including microbiology, that helps reveal paleoclimate histories and predict future climate change. Though glacier-ice microbes are studied using culture or amplicon approaches, more challenging metagenomic approaches, which provide access to functional, genome-resolved information and viruses, are under-utilized, partly due to low biomass and potential contamination. Results We expand existing clean sampling procedures using controlled artificial ice-core experiments and adapted previously established low-biomass metagenomic approaches to study glacier-ice viruses. Controlled sampling experiments drastically reduced mock contaminants including bacteria, viruses, and free DNA to background levels. Amplicon sequencing from eight depths of two Tibetan Plateau ice cores revealed common glacier-ice lineages including Janthinobacterium, Polaromonas, Herminiimonas, Flavobacterium, Sphingomonas, and Methylobacterium as the dominant genera, while microbial communities were significantly different between two ice cores, associating with different climate conditions during deposition. Separately, ~355- and ~14,400-year-old ice were subject to viral enrichment and low-input quantitative sequencing, yielding genomic sequences for 33 vOTUs. These were virtually all unique to this study, representing 28 novel genera and not a single species shared with 225 environmentally diverse viromes. Further, 42.4% of the vOTUs were identifiable temperate, which is significantly higher than that in gut, soil, and marine viromes, and indicates that temperate phages are possibly favored in glacier-ice environments before being frozen. In silico host predictions linked 18 vOTUs to co-occurring abundant bacteria (Methylobacterium, Sphingomonas, and Janthinobacterium), indicating that these phages infected ice-abundant bacterial groups before being archived. Functional genome annotation revealed four virus-encoded auxiliary metabolic genes, particularly two motility genes suggest viruses potentially facilitate nutrient acquisition for their hosts. Finally, given their possible importance to methane cycling in ice, we focused on Methylobacterium viruses by contextualizing our ice-observed viruses against 123 viromes and prophages extracted from 131 Methylobacterium genomes, revealing that the archived viruses might originate from soil or plants. Conclusions Together, these efforts further microbial and viral sampling procedures for glacier ice and provide a first window into viral communities and functions in ancient glacier environments. Such methods and datasets can potentially enable researchers to contextualize new discoveries and begin to incorporate glacier-ice microbes and their viruses relative to past and present climate change in geographically diverse regions globally.},
doi = {10.1186/s40168-021-01106-w},
journal = {Microbiome},
number = 1,
volume = 9,
place = {United States},
year = {Tue Jul 20 00:00:00 EDT 2021},
month = {Tue Jul 20 00:00:00 EDT 2021}
}
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trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
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VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences
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Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology
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Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems
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Recovery and Identification of Viable Bacteria Immured in Glacial Ice
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A mechanical role for the chemotaxis system in swarming motility
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Historically unprecedented global glacier decline in the early 21st century
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Genetic and life-history traits associated with the distribution of prophages in bacteria
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Microbially driven export of labile organic carbon from the Greenland ice sheet
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CheckV assesses the quality and completeness of metagenome-assembled viral genomes
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Metaviromics of Namib Desert Salt Pans: A Novel Lineage of Haloarchaeal Salterproviruses and a Rich Source of ssDNA Viruses
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Infecting bacteriophage Mu DNA forms a circular DNA-protein complex
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Lysogeny in nature: mechanisms, impact and ecology of temperate phages
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Bacteria variabilities in a Tibetan ice core and their relations with climate change: BACTERIA IN TIBETAN ICE CORE
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Glacial ice cores: A model system for developing extraterrestrial decontamination protocols
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Detection of tomato mosaic tobamovirus RNA in ancient glacial ice
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Geochemical and Microbiological Studies of Nitrous Oxide Variations within the New NEEM Greenland Ice Core during the Last Glacial Period
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Coexistence of phage and bacteria on the boundary of self-organized refuges
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Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons
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Metagenomic Characterisation of the Viral Community of Lough Neagh, the Largest Freshwater Lake in Ireland
journal, February 2016

Diversity of DNA and RNA Viruses in Indoor Air As Assessed via Metagenomic Sequencing
journal, January 2018

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Redefining the invertebrate RNA virosphere
journal, November 2016

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