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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Published in:PLOS ONE
Main Authors: Joy Buongiorno, Katie Sipes, Kenneth Wasmund, Alexander Loy, Karen G Lloyd
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2020
Subjects:
R
Q
Online Access:https://doi.org/10.1371/journal.pone.0234839
https://doaj.org/article/eda30990ee084971bc591184d733781f
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spelling ftdoajarticles:oai:doaj.org/article:eda30990ee084971bc591184d733781f 2023-05-15T14:54:45+02:00 Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment. Joy Buongiorno Katie Sipes Kenneth Wasmund Alexander Loy Karen G Lloyd 2020-01-01T00:00:00Z https://doi.org/10.1371/journal.pone.0234839 https://doaj.org/article/eda30990ee084971bc591184d733781f EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pone.0234839 https://doaj.org/toc/1932-6203 1932-6203 doi:10.1371/journal.pone.0234839 https://doaj.org/article/eda30990ee084971bc591184d733781f PLoS ONE, Vol 15, Iss 8, p e0234839 (2020) Medicine R Science Q article 2020 ftdoajarticles https://doi.org/10.1371/journal.pone.0234839 2022-12-31T10:01:33Z 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. Article in Journal/Newspaper Arctic Kongsfjord* Kongsfjorden Svalbard Van Keulenfjorden Directory of Open Access Journals: DOAJ Articles Arctic Svalbard Van Keulenfjorden ENVELOPE(15.489,15.489,77.559,77.559) PLOS ONE 15 8 e0234839
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Joy Buongiorno
Katie Sipes
Kenneth Wasmund
Alexander Loy
Karen G Lloyd
Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment.
topic_facet Medicine
R
Science
Q
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.
format Article in Journal/Newspaper
author Joy Buongiorno
Katie Sipes
Kenneth Wasmund
Alexander Loy
Karen G Lloyd
author_facet Joy Buongiorno
Katie Sipes
Kenneth Wasmund
Alexander Loy
Karen G Lloyd
author_sort Joy Buongiorno
title 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_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_sort woeseiales transcriptional response to shallow burial in arctic fjord surface sediment.
publisher Public Library of Science (PLoS)
publishDate 2020
url https://doi.org/10.1371/journal.pone.0234839
https://doaj.org/article/eda30990ee084971bc591184d733781f
long_lat ENVELOPE(15.489,15.489,77.559,77.559)
geographic Arctic
Svalbard
Van Keulenfjorden
geographic_facet Arctic
Svalbard
Van Keulenfjorden
genre Arctic
Kongsfjord*
Kongsfjorden
Svalbard
Van Keulenfjorden
genre_facet Arctic
Kongsfjord*
Kongsfjorden
Svalbard
Van Keulenfjorden
op_source PLoS ONE, Vol 15, Iss 8, p e0234839 (2020)
op_relation https://doi.org/10.1371/journal.pone.0234839
https://doaj.org/toc/1932-6203
1932-6203
doi:10.1371/journal.pone.0234839
https://doaj.org/article/eda30990ee084971bc591184d733781f
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