Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh
Abstract 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 mi...
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doaj-180bbefeb0594ae9b6b955b6a0763d402021-02-21T12:45:31ZengBMCMicrobiome2049-26182021-02-019111610.1186/s40168-020-00964-0Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marshDaniel R. Leadbeater0Nicola C. Oates1Joseph P. Bennett2Yi Li3Adam A. Dowle4Joe D. Taylor5Juliana Sanchez Alponti6Alexander T. Setchfield7Anna M. Alessi8Thorunn Helgason9Simon J. McQueen-Mason10Neil C. Bruce11Centre for Novel Agricultural Products, Department of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkBioscience Technology Facility, Department of Biology, University of YorkSchool of Chemistry and Biosciences, University of BradfordCentre for Novel Agricultural Products, Department of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkDepartment of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkCentre for Novel Agricultural Products, Department of Biology, University of YorkAbstract 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. Video Abstracthttps://doi.org/10.1186/s40168-020-00964-0Salt marshLignocelluloseCAZymeCarbon cyclingCarbohydrate esteraseCE1 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Daniel R. Leadbeater Nicola C. Oates Joseph P. Bennett Yi Li Adam A. Dowle Joe D. Taylor Juliana Sanchez Alponti Alexander T. Setchfield Anna M. Alessi Thorunn Helgason Simon J. McQueen-Mason Neil C. Bruce |
spellingShingle |
Daniel R. Leadbeater Nicola C. Oates Joseph P. Bennett Yi Li Adam A. Dowle Joe D. Taylor Juliana Sanchez Alponti Alexander T. Setchfield Anna M. Alessi Thorunn Helgason Simon J. McQueen-Mason Neil C. Bruce Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh Microbiome Salt marsh Lignocellulose CAZyme Carbon cycling Carbohydrate esterase CE1 |
author_facet |
Daniel R. Leadbeater Nicola C. Oates Joseph P. Bennett Yi Li Adam A. Dowle Joe D. Taylor Juliana Sanchez Alponti Alexander T. Setchfield Anna M. Alessi Thorunn Helgason Simon J. McQueen-Mason Neil C. Bruce |
author_sort |
Daniel R. Leadbeater |
title |
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_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_sort |
mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a uk salt marsh |
publisher |
BMC |
series |
Microbiome |
issn |
2049-2618 |
publishDate |
2021-02-01 |
description |
Abstract 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. Video Abstract |
topic |
Salt marsh Lignocellulose CAZyme Carbon cycling Carbohydrate esterase CE1 |
url |
https://doi.org/10.1186/s40168-020-00964-0 |
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