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Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies

BACKGROUND: Lignocellulose is one of the most abundant forms of fixed carbon in the biosphere. Current industrial approaches to the degradation of lignocellulose employ enzyme mixtures, usually from a single fungal species, which are only effective in hydrolyzing polysaccharides following biomass pr...

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Autores principales: Alessi, Anna M., Bird, Susannah M., Oates, Nicola C., Li, Yi, Dowle, Adam A., Novotny, Etelvino H., deAzevedo, Eduardo R., Bennett, Joseph P., Polikarpov, Igor, Young, J. Peter W., McQueen-Mason, Simon J., Bruce, Neil C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004670/
https://www.ncbi.nlm.nih.gov/pubmed/29946357
http://dx.doi.org/10.1186/s13068-018-1164-2
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author Alessi, Anna M.
Bird, Susannah M.
Oates, Nicola C.
Li, Yi
Dowle, Adam A.
Novotny, Etelvino H.
deAzevedo, Eduardo R.
Bennett, Joseph P.
Polikarpov, Igor
Young, J. Peter W.
McQueen-Mason, Simon J.
Bruce, Neil C.
author_facet Alessi, Anna M.
Bird, Susannah M.
Oates, Nicola C.
Li, Yi
Dowle, Adam A.
Novotny, Etelvino H.
deAzevedo, Eduardo R.
Bennett, Joseph P.
Polikarpov, Igor
Young, J. Peter W.
McQueen-Mason, Simon J.
Bruce, Neil C.
author_sort Alessi, Anna M.
collection PubMed
description BACKGROUND: Lignocellulose is one of the most abundant forms of fixed carbon in the biosphere. Current industrial approaches to the degradation of lignocellulose employ enzyme mixtures, usually from a single fungal species, which are only effective in hydrolyzing polysaccharides following biomass pre-treatments. While the enzymatic mechanisms of lignocellulose degradation have been characterized in detail in individual microbial species, the microbial communities that efficiently breakdown plant materials in nature are species rich and secrete a myriad of enzymes to perform “community-level” metabolism of lignocellulose. Single-species approaches are, therefore, likely to miss important aspects of lignocellulose degradation that will be central to optimizing commercial processes. RESULTS: Here, we investigated the microbial degradation of wheat straw in liquid cultures that had been inoculated with wheat straw compost. Samples taken at selected time points were subjected to multi-omics analysis with the aim of identifying new microbial mechanisms for lignocellulose degradation that could be applied in industrial pre-treatment of feedstocks. Phylogenetic composition of the community, based on sequenced bacterial and eukaryotic ribosomal genes, showed a gradual decrease in complexity and diversity over time due to microbial enrichment. Taxonomic affiliation of bacterial species showed dominance of Bacteroidetes and Proteobacteria and high relative abundance of genera Asticcacaulis, Leadbetterella and Truepera. The eukaryotic members of the community were enriched in peritrich ciliates from genus Telotrochidium that thrived in the liquid cultures compared to fungal species that were present in low abundance. A targeted metasecretome approach combined with metatranscriptomics analysis, identified 1127 proteins and showed the presence of numerous carbohydrate-active enzymes extracted from the biomass-bound fractions and from the culture supernatant. This revealed a wide array of hydrolytic cellulases, hemicellulases and carbohydrate-binding modules involved in lignocellulose degradation. The expression of these activities correlated to the changes in the biomass composition observed by FTIR and ssNMR measurements. CONCLUSIONS: A combination of mass spectrometry-based proteomics coupled with metatranscriptomics has enabled the identification of a large number of lignocellulose degrading enzymes that can now be further explored for the development of improved enzyme cocktails for the treatment of plant-based feedstocks. In addition to the expected carbohydrate-active enzymes, our studies reveal a large number of unknown proteins, some of which may play a crucial role in community-based lignocellulose degradation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1164-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-60046702018-06-26 Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies Alessi, Anna M. Bird, Susannah M. Oates, Nicola C. Li, Yi Dowle, Adam A. Novotny, Etelvino H. deAzevedo, Eduardo R. Bennett, Joseph P. Polikarpov, Igor Young, J. Peter W. McQueen-Mason, Simon J. Bruce, Neil C. Biotechnol Biofuels Research BACKGROUND: Lignocellulose is one of the most abundant forms of fixed carbon in the biosphere. Current industrial approaches to the degradation of lignocellulose employ enzyme mixtures, usually from a single fungal species, which are only effective in hydrolyzing polysaccharides following biomass pre-treatments. While the enzymatic mechanisms of lignocellulose degradation have been characterized in detail in individual microbial species, the microbial communities that efficiently breakdown plant materials in nature are species rich and secrete a myriad of enzymes to perform “community-level” metabolism of lignocellulose. Single-species approaches are, therefore, likely to miss important aspects of lignocellulose degradation that will be central to optimizing commercial processes. RESULTS: Here, we investigated the microbial degradation of wheat straw in liquid cultures that had been inoculated with wheat straw compost. Samples taken at selected time points were subjected to multi-omics analysis with the aim of identifying new microbial mechanisms for lignocellulose degradation that could be applied in industrial pre-treatment of feedstocks. Phylogenetic composition of the community, based on sequenced bacterial and eukaryotic ribosomal genes, showed a gradual decrease in complexity and diversity over time due to microbial enrichment. Taxonomic affiliation of bacterial species showed dominance of Bacteroidetes and Proteobacteria and high relative abundance of genera Asticcacaulis, Leadbetterella and Truepera. The eukaryotic members of the community were enriched in peritrich ciliates from genus Telotrochidium that thrived in the liquid cultures compared to fungal species that were present in low abundance. A targeted metasecretome approach combined with metatranscriptomics analysis, identified 1127 proteins and showed the presence of numerous carbohydrate-active enzymes extracted from the biomass-bound fractions and from the culture supernatant. This revealed a wide array of hydrolytic cellulases, hemicellulases and carbohydrate-binding modules involved in lignocellulose degradation. The expression of these activities correlated to the changes in the biomass composition observed by FTIR and ssNMR measurements. CONCLUSIONS: A combination of mass spectrometry-based proteomics coupled with metatranscriptomics has enabled the identification of a large number of lignocellulose degrading enzymes that can now be further explored for the development of improved enzyme cocktails for the treatment of plant-based feedstocks. In addition to the expected carbohydrate-active enzymes, our studies reveal a large number of unknown proteins, some of which may play a crucial role in community-based lignocellulose degradation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1164-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-06-18 /pmc/articles/PMC6004670/ /pubmed/29946357 http://dx.doi.org/10.1186/s13068-018-1164-2 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 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.
spellingShingle Research
Alessi, Anna M.
Bird, Susannah M.
Oates, Nicola C.
Li, Yi
Dowle, Adam A.
Novotny, Etelvino H.
deAzevedo, Eduardo R.
Bennett, Joseph P.
Polikarpov, Igor
Young, J. Peter W.
McQueen-Mason, Simon J.
Bruce, Neil C.
Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
title Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
title_full Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
title_fullStr Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
title_full_unstemmed Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
title_short Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
title_sort defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004670/
https://www.ncbi.nlm.nih.gov/pubmed/29946357
http://dx.doi.org/10.1186/s13068-018-1164-2
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