Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems

BACKGROUND: Soil is an important reservoir of antibiotic resistance genes (ARGs), but their potential risk in different ecosystems as well as response to anthropogenic land use change is unknown. We used a metagenomic approach and datasets with well-characterized metadata to investigate ARG types an...

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Published in:Microbiome
Main Authors: Qian, Xun, Gunturu, Santosh, Guo, Jiarong, Chai, Benli, Cole, James R., Gu, Jie, Tiedje, James M.
Format: Text
Language:English
Published: BioMed Central 2021
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8122544/
http://www.ncbi.nlm.nih.gov/pubmed/33990222
https://doi.org/10.1186/s40168-021-01047-4
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spelling ftpubmed:oai:pubmedcentral.nih.gov:8122544 2023-05-15T18:40:20+02:00 Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems Qian, Xun Gunturu, Santosh Guo, Jiarong Chai, Benli Cole, James R. Gu, Jie Tiedje, James M. 2021-05-14 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8122544/ http://www.ncbi.nlm.nih.gov/pubmed/33990222 https://doi.org/10.1186/s40168-021-01047-4 en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8122544/ http://www.ncbi.nlm.nih.gov/pubmed/33990222 http://dx.doi.org/10.1186/s40168-021-01047-4 © 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/s40168-021-01047-4 2021-05-23T00:35:21Z BACKGROUND: Soil is an important reservoir of antibiotic resistance genes (ARGs), but their potential risk in different ecosystems as well as response to anthropogenic land use change is unknown. We used a metagenomic approach and datasets with well-characterized metadata to investigate ARG types and amounts in soil DNA of three native ecosystems: Alaskan tundra, US Midwestern prairie, and Amazon rainforest, as well as the effect of conversion of the latter two to agriculture and pasture, respectively. RESULTS: High diversity (242 ARG subtypes) and abundance (0.184–0.242 ARG copies per 16S rRNA gene copy) were observed irrespective of ecosystem, with multidrug resistance and efflux pump the dominant class and mechanism. Ten regulatory genes were identified and they accounted for 13–35% of resistome abundances in soils, among them arlR, cpxR, ompR, vanR, and vanS were dominant and observed in all studied soils. We identified 55 non-regulatory ARGs shared by all 26 soil metagenomes of the three ecosystems, which accounted for more than 81% of non-regulatory resistome abundance. Proteobacteria, Firmicutes, and Actinobacteria were primary ARG hosts, 7 of 10 most abundant ARGs were found in all of them. No significant differences in both ARG diversity and abundance were observed between native prairie soil and adjacent long-term cultivated agriculture soil. We chose 12 clinically important ARGs to evaluate at the sequence level and found them to be distinct from those in human pathogens, and when assembled they were even more dissimilar. Significant correlation was found between bacterial community structure and resistome profile, suggesting that variance in resistome profile was mainly driven by the bacterial community composition. CONCLUSIONS: Our results identify candidate background ARGs (shared in all 26 soils), classify ARG hosts, quantify resistance classes, and provide quantitative and sequence information suggestive of very low risk but also revealing resistance gene variants that might emerge in the future. ... Text Tundra PubMed Central (PMC) Microbiome 9 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research
spellingShingle Research
Qian, Xun
Gunturu, Santosh
Guo, Jiarong
Chai, Benli
Cole, James R.
Gu, Jie
Tiedje, James M.
Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
topic_facet Research
description BACKGROUND: Soil is an important reservoir of antibiotic resistance genes (ARGs), but their potential risk in different ecosystems as well as response to anthropogenic land use change is unknown. We used a metagenomic approach and datasets with well-characterized metadata to investigate ARG types and amounts in soil DNA of three native ecosystems: Alaskan tundra, US Midwestern prairie, and Amazon rainforest, as well as the effect of conversion of the latter two to agriculture and pasture, respectively. RESULTS: High diversity (242 ARG subtypes) and abundance (0.184–0.242 ARG copies per 16S rRNA gene copy) were observed irrespective of ecosystem, with multidrug resistance and efflux pump the dominant class and mechanism. Ten regulatory genes were identified and they accounted for 13–35% of resistome abundances in soils, among them arlR, cpxR, ompR, vanR, and vanS were dominant and observed in all studied soils. We identified 55 non-regulatory ARGs shared by all 26 soil metagenomes of the three ecosystems, which accounted for more than 81% of non-regulatory resistome abundance. Proteobacteria, Firmicutes, and Actinobacteria were primary ARG hosts, 7 of 10 most abundant ARGs were found in all of them. No significant differences in both ARG diversity and abundance were observed between native prairie soil and adjacent long-term cultivated agriculture soil. We chose 12 clinically important ARGs to evaluate at the sequence level and found them to be distinct from those in human pathogens, and when assembled they were even more dissimilar. Significant correlation was found between bacterial community structure and resistome profile, suggesting that variance in resistome profile was mainly driven by the bacterial community composition. CONCLUSIONS: Our results identify candidate background ARGs (shared in all 26 soils), classify ARG hosts, quantify resistance classes, and provide quantitative and sequence information suggestive of very low risk but also revealing resistance gene variants that might emerge in the future. ...
format Text
author Qian, Xun
Gunturu, Santosh
Guo, Jiarong
Chai, Benli
Cole, James R.
Gu, Jie
Tiedje, James M.
author_facet Qian, Xun
Gunturu, Santosh
Guo, Jiarong
Chai, Benli
Cole, James R.
Gu, Jie
Tiedje, James M.
author_sort Qian, Xun
title Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
title_short Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
title_full Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
title_fullStr Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
title_full_unstemmed Metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
title_sort metagenomic analysis reveals the shared and distinct features of the soil resistome across tundra, temperate prairie, and tropical ecosystems
publisher BioMed Central
publishDate 2021
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8122544/
http://www.ncbi.nlm.nih.gov/pubmed/33990222
https://doi.org/10.1186/s40168-021-01047-4
genre Tundra
genre_facet Tundra
op_source Microbiome
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8122544/
http://www.ncbi.nlm.nih.gov/pubmed/33990222
http://dx.doi.org/10.1186/s40168-021-01047-4
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.
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