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Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh

BACKGROUND: Salt marshes are major natural repositories of sequestered organic carbon with high burial rates of organic matter, produced by highly productive native flora. Accumulated carbon predominantly exists as lignocellulose which is metabolised by communities of functionally diverse microbes....

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Autores principales: Leadbeater, Daniel R., Oates, Nicola C., Bennett, Joseph P., Li, Yi, Dowle, Adam A., Taylor, Joe D., Alponti, Juliana Sanchez, Setchfield, Alexander T., Alessi, Anna M., Helgason, Thorunn, McQueen-Mason, Simon J., Bruce, Neil C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7890819/
https://www.ncbi.nlm.nih.gov/pubmed/33597033
http://dx.doi.org/10.1186/s40168-020-00964-0
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author Leadbeater, Daniel R.
Oates, Nicola C.
Bennett, Joseph P.
Li, Yi
Dowle, Adam A.
Taylor, Joe D.
Alponti, Juliana Sanchez
Setchfield, Alexander T.
Alessi, Anna M.
Helgason, Thorunn
McQueen-Mason, Simon J.
Bruce, Neil C.
author_facet Leadbeater, Daniel R.
Oates, Nicola C.
Bennett, Joseph P.
Li, Yi
Dowle, Adam A.
Taylor, Joe D.
Alponti, Juliana Sanchez
Setchfield, Alexander T.
Alessi, Anna M.
Helgason, Thorunn
McQueen-Mason, Simon J.
Bruce, Neil C.
author_sort Leadbeater, Daniel R.
collection PubMed
description BACKGROUND: Salt marshes are major natural repositories of sequestered organic carbon with high burial rates of organic matter, produced by highly productive native flora. Accumulated carbon predominantly exists as lignocellulose which is metabolised by communities of functionally diverse microbes. However, the organisms that orchestrate this process and the enzymatic mechanisms employed that regulate the accumulation, composition and permanence of this carbon stock are not yet known. We applied meta-exo-proteome proteomics and 16S rRNA gene profiling to study lignocellulose decomposition in situ within the surface level sediments of a natural established UK salt marsh. RESULTS: Our studies revealed a community dominated by Gammaproteobacteria, Bacteroidetes and Deltaproteobacteria that drive lignocellulose degradation in the salt marsh. We identify 42 families of lignocellulolytic bacteria of which the most active secretors of carbohydrate-active enzymes were observed to be Prolixibacteracea, Flavobacteriaceae, Cellvibrionaceae, Saccharospirillaceae, Alteromonadaceae, Vibrionaceae and Cytophagaceae. These families secreted lignocellulose-active glycoside hydrolase (GH) family enzymes GH3, GH5, GH6, GH9, GH10, GH11, GH13 and GH43 that were associated with degrading Spartina biomass. While fungi were present, we did not detect a lignocellulolytic contribution from fungi which are major contributors to terrestrial lignocellulose deconstruction. Oxidative enzymes such as laccases, peroxidases and lytic polysaccharide monooxygenases that are important for lignocellulose degradation in the terrestrial environment were present but not abundant, while a notable abundance of putative esterases (such as carbohydrate esterase family 1) associated with decoupling lignin from polysaccharides in lignocellulose was observed. CONCLUSIONS: Here, we identify a diverse cohort of previously undefined bacteria that drive lignocellulose degradation in the surface sediments of the salt marsh environment and describe the enzymatic mechanisms they employ to facilitate this process. Our results increase the understanding of the microbial and molecular mechanisms that underpin carbon sequestration from lignocellulose within salt marsh surface sediments in situ and provide insights into the potential enzymatic mechanisms regulating the enrichment of polyphenolics in salt marsh sediments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-020-00964-0.
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spelling pubmed-78908192021-02-22 Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh Leadbeater, Daniel R. Oates, Nicola C. Bennett, Joseph P. Li, Yi Dowle, Adam A. Taylor, Joe D. Alponti, Juliana Sanchez Setchfield, Alexander T. Alessi, Anna M. Helgason, Thorunn McQueen-Mason, Simon J. Bruce, Neil C. Microbiome Research BACKGROUND: Salt marshes are major natural repositories of sequestered organic carbon with high burial rates of organic matter, produced by highly productive native flora. Accumulated carbon predominantly exists as lignocellulose which is metabolised by communities of functionally diverse microbes. However, the organisms that orchestrate this process and the enzymatic mechanisms employed that regulate the accumulation, composition and permanence of this carbon stock are not yet known. We applied meta-exo-proteome proteomics and 16S rRNA gene profiling to study lignocellulose decomposition in situ within the surface level sediments of a natural established UK salt marsh. RESULTS: Our studies revealed a community dominated by Gammaproteobacteria, Bacteroidetes and Deltaproteobacteria that drive lignocellulose degradation in the salt marsh. We identify 42 families of lignocellulolytic bacteria of which the most active secretors of carbohydrate-active enzymes were observed to be Prolixibacteracea, Flavobacteriaceae, Cellvibrionaceae, Saccharospirillaceae, Alteromonadaceae, Vibrionaceae and Cytophagaceae. These families secreted lignocellulose-active glycoside hydrolase (GH) family enzymes GH3, GH5, GH6, GH9, GH10, GH11, GH13 and GH43 that were associated with degrading Spartina biomass. While fungi were present, we did not detect a lignocellulolytic contribution from fungi which are major contributors to terrestrial lignocellulose deconstruction. Oxidative enzymes such as laccases, peroxidases and lytic polysaccharide monooxygenases that are important for lignocellulose degradation in the terrestrial environment were present but not abundant, while a notable abundance of putative esterases (such as carbohydrate esterase family 1) associated with decoupling lignin from polysaccharides in lignocellulose was observed. CONCLUSIONS: Here, we identify a diverse cohort of previously undefined bacteria that drive lignocellulose degradation in the surface sediments of the salt marsh environment and describe the enzymatic mechanisms they employ to facilitate this process. Our results increase the understanding of the microbial and molecular mechanisms that underpin carbon sequestration from lignocellulose within salt marsh surface sediments in situ and provide insights into the potential enzymatic mechanisms regulating the enrichment of polyphenolics in salt marsh sediments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-020-00964-0. BioMed Central 2021-02-17 /pmc/articles/PMC7890819/ /pubmed/33597033 http://dx.doi.org/10.1186/s40168-020-00964-0 Text en © The Author(s) 2021 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/. The Creative Commons Public Domain Dedication waiver (http://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.
spellingShingle Research
Leadbeater, Daniel R.
Oates, Nicola C.
Bennett, Joseph P.
Li, Yi
Dowle, Adam A.
Taylor, Joe D.
Alponti, Juliana Sanchez
Setchfield, Alexander T.
Alessi, Anna M.
Helgason, Thorunn
McQueen-Mason, Simon J.
Bruce, Neil C.
Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
title Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
title_full Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
title_fullStr Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
title_full_unstemmed Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
title_short Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
title_sort mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a uk salt marsh
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7890819/
https://www.ncbi.nlm.nih.gov/pubmed/33597033
http://dx.doi.org/10.1186/s40168-020-00964-0
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