Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution

BACKGROUND: Microorganisms drive critical global biogeochemical cycles and dominate the biomass in Earth’s expansive cold biosphere. Determining the genomic traits that enable psychrophiles to grow in cold environments informs about their physiology and adaptive responses. However, defining importan...

Full description

Bibliographic Details
Published in:Microbiome
Main Authors: Shen, Liang, Liu, Yongqin, Allen, Michelle A., Xu, Baiqing, Wang, Ninglian, Williams, Timothy J., Wang, Feng, Zhou, Yuguang, Liu, Qing, Cavicchioli, Ricardo
Format: Text
Language:English
Published: BioMed Central 2021
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8196931/
http://www.ncbi.nlm.nih.gov/pubmed/34118971
https://doi.org/10.1186/s40168-021-01084-z
id ftpubmed:oai:pubmedcentral.nih.gov:8196931
record_format openpolar
spelling ftpubmed:oai:pubmedcentral.nih.gov:8196931 2023-05-15T17:57:58+02:00 Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang Liu, Yongqin Allen, Michelle A. Xu, Baiqing Wang, Ninglian Williams, Timothy J. Wang, Feng Zhou, Yuguang Liu, Qing Cavicchioli, Ricardo 2021-06-12 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8196931/ http://www.ncbi.nlm.nih.gov/pubmed/34118971 https://doi.org/10.1186/s40168-021-01084-z en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8196931/ http://www.ncbi.nlm.nih.gov/pubmed/34118971 http://dx.doi.org/10.1186/s40168-021-01084-z © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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. CC0 PDM CC-BY Microbiome Research Text 2021 ftpubmed https://doi.org/10.1186/s40168-021-01084-z 2021-06-20T00:40:32Z BACKGROUND: Microorganisms drive critical global biogeochemical cycles and dominate the biomass in Earth’s expansive cold biosphere. Determining the genomic traits that enable psychrophiles to grow in cold environments informs about their physiology and adaptive responses. However, defining important genomic traits of psychrophiles has proven difficult, with the ability to extrapolate genomic knowledge to environmental relevance proving even more difficult. RESULTS: Here we examined the bacterial genus Arthrobacter and, assisted by genome sequences of new Tibetan Plateau isolates, defined a new clade, Group C, that represents isolates from polar and alpine environments. Group C had a superior ability to grow at −1°C and possessed genome G+C content, amino acid composition, predicted protein stability, and functional capacities (e.g., sulfur metabolism and mycothiol biosynthesis) that distinguished it from non-polar or alpine Group A Arthrobacter. Interrogation of nearly 1000 metagenomes identified an over-representation of Group C in Canadian permafrost communities from a simulated spring-thaw experiment, indicative of niche adaptation, and an under-representation of Group A in all polar and alpine samples, indicative of a general response to environmental temperature. CONCLUSION: The findings illustrate a capacity to define genomic markers of specific taxa that potentially have value for environmental monitoring of cold environments, including environmental change arising from anthropogenic impact. More broadly, the study illustrates the challenges involved in extrapolating from genomic and physiological data to an environmental setting. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01084-z. Text permafrost PubMed Central (PMC) Microbiome 9 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research
spellingShingle Research
Shen, Liang
Liu, Yongqin
Allen, Michelle A.
Xu, Baiqing
Wang, Ninglian
Williams, Timothy J.
Wang, Feng
Zhou, Yuguang
Liu, Qing
Cavicchioli, Ricardo
Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution
topic_facet Research
description BACKGROUND: Microorganisms drive critical global biogeochemical cycles and dominate the biomass in Earth’s expansive cold biosphere. Determining the genomic traits that enable psychrophiles to grow in cold environments informs about their physiology and adaptive responses. However, defining important genomic traits of psychrophiles has proven difficult, with the ability to extrapolate genomic knowledge to environmental relevance proving even more difficult. RESULTS: Here we examined the bacterial genus Arthrobacter and, assisted by genome sequences of new Tibetan Plateau isolates, defined a new clade, Group C, that represents isolates from polar and alpine environments. Group C had a superior ability to grow at −1°C and possessed genome G+C content, amino acid composition, predicted protein stability, and functional capacities (e.g., sulfur metabolism and mycothiol biosynthesis) that distinguished it from non-polar or alpine Group A Arthrobacter. Interrogation of nearly 1000 metagenomes identified an over-representation of Group C in Canadian permafrost communities from a simulated spring-thaw experiment, indicative of niche adaptation, and an under-representation of Group A in all polar and alpine samples, indicative of a general response to environmental temperature. CONCLUSION: The findings illustrate a capacity to define genomic markers of specific taxa that potentially have value for environmental monitoring of cold environments, including environmental change arising from anthropogenic impact. More broadly, the study illustrates the challenges involved in extrapolating from genomic and physiological data to an environmental setting. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01084-z.
format Text
author Shen, Liang
Liu, Yongqin
Allen, Michelle A.
Xu, Baiqing
Wang, Ninglian
Williams, Timothy J.
Wang, Feng
Zhou, Yuguang
Liu, Qing
Cavicchioli, Ricardo
author_facet Shen, Liang
Liu, Yongqin
Allen, Michelle A.
Xu, Baiqing
Wang, Ninglian
Williams, Timothy J.
Wang, Feng
Zhou, Yuguang
Liu, Qing
Cavicchioli, Ricardo
author_sort Shen, Liang
title Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution
title_short Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution
title_full Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution
title_fullStr Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution
title_full_unstemmed Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution
title_sort linking genomic and physiological characteristics of psychrophilic arthrobacter to metagenomic data to explain global environmental distribution
publisher BioMed Central
publishDate 2021
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8196931/
http://www.ncbi.nlm.nih.gov/pubmed/34118971
https://doi.org/10.1186/s40168-021-01084-z
genre permafrost
genre_facet permafrost
op_source Microbiome
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8196931/
http://www.ncbi.nlm.nih.gov/pubmed/34118971
http://dx.doi.org/10.1186/s40168-021-01084-z
op_rights © The Author(s) 2021
https://creativecommons.org/licenses/by/4.0/Open AccessThis 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_rightsnorm CC0
PDM
CC-BY
op_doi https://doi.org/10.1186/s40168-021-01084-z
container_title Microbiome
container_volume 9
container_issue 1
_version_ 1766166491569324032