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

Abstract 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...

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Published in:Microbiome
Main Authors: Thomas Grevesse, Céline Guéguen, Vera E. Onana, David A. Walsh
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2022
Subjects:
Online Access:https://doi.org/10.1186/s40168-022-01417-6
https://doaj.org/article/1cf3204967a5495fa4d28d36e7f84723
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spelling ftdoajarticles:oai:doaj.org/article:1cf3204967a5495fa4d28d36e7f84723 2023-05-15T14:43:24+02:00 Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes Thomas Grevesse Céline Guéguen Vera E. Onana David A. Walsh 2022-12-01T00:00:00Z https://doi.org/10.1186/s40168-022-01417-6 https://doaj.org/article/1cf3204967a5495fa4d28d36e7f84723 EN eng BMC https://doi.org/10.1186/s40168-022-01417-6 https://doaj.org/toc/2049-2618 doi:10.1186/s40168-022-01417-6 2049-2618 https://doaj.org/article/1cf3204967a5495fa4d28d36e7f84723 Microbiome, Vol 10, Iss 1, Pp 1-21 (2022) Microbial ecology QR100-130 article 2022 ftdoajarticles https://doi.org/10.1186/s40168-022-01417-6 2023-03-26T01:32:49Z Abstract 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 ... Article in Journal/Newspaper Arctic Arctic Ocean canada basin Global warming permafrost Directory of Open Access Journals: DOAJ Articles Arctic Arctic Ocean Canada Microbiome 10 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Microbial ecology
QR100-130
spellingShingle Microbial ecology
QR100-130
Thomas Grevesse
Céline Guéguen
Vera E. Onana
David A. Walsh
Degradation pathways for organic matter of terrestrial origin are widespread and expressed in Arctic Ocean microbiomes
topic_facet Microbial ecology
QR100-130
description Abstract 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 ...
format Article in Journal/Newspaper
author Thomas Grevesse
Céline Guéguen
Vera E. Onana
David A. Walsh
author_facet Thomas Grevesse
Céline Guéguen
Vera E. Onana
David A. Walsh
author_sort Thomas Grevesse
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 BMC
publishDate 2022
url https://doi.org/10.1186/s40168-022-01417-6
https://doaj.org/article/1cf3204967a5495fa4d28d36e7f84723
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, Vol 10, Iss 1, Pp 1-21 (2022)
op_relation https://doi.org/10.1186/s40168-022-01417-6
https://doaj.org/toc/2049-2618
doi:10.1186/s40168-022-01417-6
2049-2618
https://doaj.org/article/1cf3204967a5495fa4d28d36e7f84723
op_doi https://doi.org/10.1186/s40168-022-01417-6
container_title Microbiome
container_volume 10
container_issue 1
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