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Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment

Distinct lineages of Gammaproteobacteria clade Woeseiales are globally distributed in marine sediments, based on metagenomic and 16S rRNA gene analysis. Yet little is known about why they are dominant or their ecological role in Arctic fjord sediments, where glacial retreat is rapidly imposing chang...

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Autores principales: Buongiorno, Joy, Sipes, Katie, Wasmund, Kenneth, Loy, Alexander, Lloyd, Karen G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7451513/
https://www.ncbi.nlm.nih.gov/pubmed/32853201
http://dx.doi.org/10.1371/journal.pone.0234839
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author Buongiorno, Joy
Sipes, Katie
Wasmund, Kenneth
Loy, Alexander
Lloyd, Karen G.
author_facet Buongiorno, Joy
Sipes, Katie
Wasmund, Kenneth
Loy, Alexander
Lloyd, Karen G.
author_sort Buongiorno, Joy
collection PubMed
description Distinct lineages of Gammaproteobacteria clade Woeseiales are globally distributed in marine sediments, based on metagenomic and 16S rRNA gene analysis. Yet little is known about why they are dominant or their ecological role in Arctic fjord sediments, where glacial retreat is rapidly imposing change. This study combined 16S rRNA gene analysis, metagenome-assembled genomes (MAGs), and genome-resolved metatranscriptomics uncovered the in situ abundance and transcriptional activity of Woeseiales with burial in four shallow sediment sites of Kongsfjorden and Van Keulenfjorden of Svalbard (79°N). We present five novel Woeseiales MAGs and show transcriptional evidence for metabolic plasticity during burial, including sulfur oxidation with reverse dissimilatory sulfite reductase (dsrAB) down to 4 cm depth and nitrite reduction down to 6 cm depth. A single stress protein, spore protein SP21 (hspA), had a tenfold higher mRNA abundance than any other transcript, and was a hundredfold higher on average than other transcripts. At three out of the four sites, SP21 transcript abundance increased with depth, while total mRNA abundance and richness decreased, indicating a shift in investment from metabolism and other cellular processes to build-up of spore protein SP21. The SP21 gene in MAGs was often flanked by genes involved in membrane-associated stress response. The ability of Woeseiales to shift from sulfur oxidation to nitrite reduction with burial into marine sediments with decreasing access to overlying oxic bottom waters, as well as enter into a dormant state dominated by SP21, may account for its ubiquity and high abundance in marine sediments worldwide, including those of the rapidly shifting Arctic.
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spelling pubmed-74515132020-09-02 Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment Buongiorno, Joy Sipes, Katie Wasmund, Kenneth Loy, Alexander Lloyd, Karen G. PLoS One Research Article Distinct lineages of Gammaproteobacteria clade Woeseiales are globally distributed in marine sediments, based on metagenomic and 16S rRNA gene analysis. Yet little is known about why they are dominant or their ecological role in Arctic fjord sediments, where glacial retreat is rapidly imposing change. This study combined 16S rRNA gene analysis, metagenome-assembled genomes (MAGs), and genome-resolved metatranscriptomics uncovered the in situ abundance and transcriptional activity of Woeseiales with burial in four shallow sediment sites of Kongsfjorden and Van Keulenfjorden of Svalbard (79°N). We present five novel Woeseiales MAGs and show transcriptional evidence for metabolic plasticity during burial, including sulfur oxidation with reverse dissimilatory sulfite reductase (dsrAB) down to 4 cm depth and nitrite reduction down to 6 cm depth. A single stress protein, spore protein SP21 (hspA), had a tenfold higher mRNA abundance than any other transcript, and was a hundredfold higher on average than other transcripts. At three out of the four sites, SP21 transcript abundance increased with depth, while total mRNA abundance and richness decreased, indicating a shift in investment from metabolism and other cellular processes to build-up of spore protein SP21. The SP21 gene in MAGs was often flanked by genes involved in membrane-associated stress response. The ability of Woeseiales to shift from sulfur oxidation to nitrite reduction with burial into marine sediments with decreasing access to overlying oxic bottom waters, as well as enter into a dormant state dominated by SP21, may account for its ubiquity and high abundance in marine sediments worldwide, including those of the rapidly shifting Arctic. Public Library of Science 2020-08-27 /pmc/articles/PMC7451513/ /pubmed/32853201 http://dx.doi.org/10.1371/journal.pone.0234839 Text en © 2020 Buongiorno et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Buongiorno, Joy
Sipes, Katie
Wasmund, Kenneth
Loy, Alexander
Lloyd, Karen G.
Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment
title Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment
title_full Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment
title_fullStr Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment
title_full_unstemmed Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment
title_short Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment
title_sort woeseiales transcriptional response to shallow burial in arctic fjord surface sediment
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7451513/
https://www.ncbi.nlm.nih.gov/pubmed/32853201
http://dx.doi.org/10.1371/journal.pone.0234839
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