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Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders

Macroalgae represent huge amounts of biomass worldwide, largely recycled by marine heterotrophic bacteria. We investigated the strategies of bacteria within the flavobacterial genus Zobellia to initiate the degradation of whole algal tissues, which has received little attention compared to the degra...

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Autores principales: Brunet, Maéva, Le Duff, Nolwen, Barbeyron, Tristan, Thomas, François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9296495/
https://www.ncbi.nlm.nih.gov/pubmed/35589967
http://dx.doi.org/10.1038/s41396-022-01251-6
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author Brunet, Maéva
Le Duff, Nolwen
Barbeyron, Tristan
Thomas, François
author_facet Brunet, Maéva
Le Duff, Nolwen
Barbeyron, Tristan
Thomas, François
author_sort Brunet, Maéva
collection PubMed
description Macroalgae represent huge amounts of biomass worldwide, largely recycled by marine heterotrophic bacteria. We investigated the strategies of bacteria within the flavobacterial genus Zobellia to initiate the degradation of whole algal tissues, which has received little attention compared to the degradation of isolated polysaccharides. Zobellia galactanivorans Dsij(T) has the capacity to use fresh brown macroalgae as a sole carbon source and extensively degrades algal tissues via the secretion of extracellular enzymes, even in the absence of physical contact with the algae. Co-cultures experiments with the non-degrading strain Tenacibaculum aestuarii SMK-4(T) showed that Z. galactanivorans can act as a pioneer that initiates algal breakdown and shares public goods with other bacteria. A comparison of eight Zobellia strains, and strong transcriptomic shifts in Z. galactanivorans cells using fresh macroalgae vs. isolated polysaccharides, revealed potential overlooked traits of pioneer bacteria. Besides brown algal polysaccharide degradation, they notably include oxidative stress resistance proteins, type IX secretion system proteins and novel uncharacterized polysaccharide utilization loci. Overall, this work highlights the relevance of studying fresh macroalga degradation to fully understand the metabolic and ecological strategies of pioneer microbial degraders, key players in macroalgal biomass remineralization.
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spelling pubmed-92964952022-07-21 Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders Brunet, Maéva Le Duff, Nolwen Barbeyron, Tristan Thomas, François ISME J Article Macroalgae represent huge amounts of biomass worldwide, largely recycled by marine heterotrophic bacteria. We investigated the strategies of bacteria within the flavobacterial genus Zobellia to initiate the degradation of whole algal tissues, which has received little attention compared to the degradation of isolated polysaccharides. Zobellia galactanivorans Dsij(T) has the capacity to use fresh brown macroalgae as a sole carbon source and extensively degrades algal tissues via the secretion of extracellular enzymes, even in the absence of physical contact with the algae. Co-cultures experiments with the non-degrading strain Tenacibaculum aestuarii SMK-4(T) showed that Z. galactanivorans can act as a pioneer that initiates algal breakdown and shares public goods with other bacteria. A comparison of eight Zobellia strains, and strong transcriptomic shifts in Z. galactanivorans cells using fresh macroalgae vs. isolated polysaccharides, revealed potential overlooked traits of pioneer bacteria. Besides brown algal polysaccharide degradation, they notably include oxidative stress resistance proteins, type IX secretion system proteins and novel uncharacterized polysaccharide utilization loci. Overall, this work highlights the relevance of studying fresh macroalga degradation to fully understand the metabolic and ecological strategies of pioneer microbial degraders, key players in macroalgal biomass remineralization. Nature Publishing Group UK 2022-05-19 2022-08 /pmc/articles/PMC9296495/ /pubmed/35589967 http://dx.doi.org/10.1038/s41396-022-01251-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Brunet, Maéva
Le Duff, Nolwen
Barbeyron, Tristan
Thomas, François
Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders
title Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders
title_full Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders
title_fullStr Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders
title_full_unstemmed Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders
title_short Consuming fresh macroalgae induces specific catabolic pathways, stress reactions and Type IX secretion in marine flavobacterial pioneer degraders
title_sort consuming fresh macroalgae induces specific catabolic pathways, stress reactions and type ix secretion in marine flavobacterial pioneer degraders
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9296495/
https://www.ncbi.nlm.nih.gov/pubmed/35589967
http://dx.doi.org/10.1038/s41396-022-01251-6
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