Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes

BACKGROUND: The Arctic Ocean receives massive freshwater input and a correspondingly large amount of humic-rich organic matter of terrestrial origin. Global warming, permafrost melt, and a changing hydrological cycle will contribute to an intensification of terrestrial organic matter release to the...

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Published in:Microbiome
Main Authors: Grevesse, Thomas, Guéguen, Céline, Onana, Vera E., Walsh, David A.
Format: Text
Language:English
Published: BioMed Central 2022
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789639/
http://www.ncbi.nlm.nih.gov/pubmed/36566218
https://doi.org/10.1186/s40168-022-01417-6
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spelling ftpubmed:oai:pubmedcentral.nih.gov:9789639 2023-05-15T14:43:21+02:00 Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes Grevesse, Thomas Guéguen, Céline Onana, Vera E. Walsh, David A. 2022-12-24 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789639/ http://www.ncbi.nlm.nih.gov/pubmed/36566218 https://doi.org/10.1186/s40168-022-01417-6 en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789639/ http://www.ncbi.nlm.nih.gov/pubmed/36566218 http://dx.doi.org/10.1186/s40168-022-01417-6 © The Author(s) 2022 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 2022 ftpubmed https://doi.org/10.1186/s40168-022-01417-6 2023-01-01T01:36:55Z BACKGROUND: The Arctic Ocean receives massive freshwater input and a correspondingly large amount of humic-rich organic matter of terrestrial origin. Global warming, permafrost melt, and a changing hydrological cycle will contribute to an intensification of terrestrial organic matter release to the Arctic Ocean. Although considered recalcitrant to degradation due to complex aromatic structures, humic substances can serve as substrate for microbial growth in terrestrial environments. However, the capacity of marine microbiomes to process aromatic-rich humic substances, and how this processing may contribute to carbon and nutrient cycling in a changing Arctic Ocean, is relatively unexplored. Here, we used a combination of metagenomics and metatranscriptomics to assess the prevalence and diversity of metabolic pathways and bacterial taxa involved in aromatic compound degradation in the salinity-stratified summer waters of the Canada Basin in the western Arctic Ocean. RESULTS: Community-scale meta-omics profiling revealed that 22 complete pathways for processing aromatic compounds were present and expressed in the Canada Basin, including those for aromatic ring fission and upstream funneling pathways to access diverse aromatic compounds of terrestrial origin. A phylogenetically diverse set of functional marker genes and transcripts were associated with fluorescent dissolved organic matter, a component of which is of terrestrial origin. Pathways were common throughout global ocean microbiomes but were more abundant in the Canada Basin. Genome-resolved analyses identified 12 clades of Alphaproteobacteria, including Rhodospirillales, as central contributors to aromatic compound processing. These genomes were mostly restricted in their biogeographical distribution to the Arctic Ocean and were enriched in aromatic compound processing genes compared to their closest relatives from other oceans. CONCLUSION: Overall, the detection of a phylogenetically diverse set of genes and transcripts implicated in aromatic compound ... Text Arctic Arctic Ocean canada basin Global warming permafrost PubMed Central (PMC) Arctic Arctic Ocean Canada Microbiome 10 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research
spellingShingle Research
Grevesse, Thomas
Guéguen, Céline
Onana, Vera E.
Walsh, David A.
Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
topic_facet Research
description BACKGROUND: The Arctic Ocean receives massive freshwater input and a correspondingly large amount of humic-rich organic matter of terrestrial origin. Global warming, permafrost melt, and a changing hydrological cycle will contribute to an intensification of terrestrial organic matter release to the Arctic Ocean. Although considered recalcitrant to degradation due to complex aromatic structures, humic substances can serve as substrate for microbial growth in terrestrial environments. However, the capacity of marine microbiomes to process aromatic-rich humic substances, and how this processing may contribute to carbon and nutrient cycling in a changing Arctic Ocean, is relatively unexplored. Here, we used a combination of metagenomics and metatranscriptomics to assess the prevalence and diversity of metabolic pathways and bacterial taxa involved in aromatic compound degradation in the salinity-stratified summer waters of the Canada Basin in the western Arctic Ocean. RESULTS: Community-scale meta-omics profiling revealed that 22 complete pathways for processing aromatic compounds were present and expressed in the Canada Basin, including those for aromatic ring fission and upstream funneling pathways to access diverse aromatic compounds of terrestrial origin. A phylogenetically diverse set of functional marker genes and transcripts were associated with fluorescent dissolved organic matter, a component of which is of terrestrial origin. Pathways were common throughout global ocean microbiomes but were more abundant in the Canada Basin. Genome-resolved analyses identified 12 clades of Alphaproteobacteria, including Rhodospirillales, as central contributors to aromatic compound processing. These genomes were mostly restricted in their biogeographical distribution to the Arctic Ocean and were enriched in aromatic compound processing genes compared to their closest relatives from other oceans. CONCLUSION: Overall, the detection of a phylogenetically diverse set of genes and transcripts implicated in aromatic compound ...
format Text
author Grevesse, Thomas
Guéguen, Céline
Onana, Vera E.
Walsh, David A.
author_facet Grevesse, Thomas
Guéguen, Céline
Onana, Vera E.
Walsh, David A.
author_sort Grevesse, Thomas
title Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
title_short Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
title_full Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
title_fullStr Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
title_full_unstemmed Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
title_sort degradation pathways for organic matter of terrestrial origin are widespread and expressed in arctic ocean microbiomes
publisher BioMed Central
publishDate 2022
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789639/
http://www.ncbi.nlm.nih.gov/pubmed/36566218
https://doi.org/10.1186/s40168-022-01417-6
geographic Arctic
Arctic Ocean
Canada
geographic_facet Arctic
Arctic Ocean
Canada
genre Arctic
Arctic Ocean
canada basin
Global warming
permafrost
genre_facet Arctic
Arctic Ocean
canada basin
Global warming
permafrost
op_source Microbiome
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9789639/
http://www.ncbi.nlm.nih.gov/pubmed/36566218
http://dx.doi.org/10.1186/s40168-022-01417-6
op_rights © The Author(s) 2022
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/s40168-022-01417-6
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