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Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study

BACKGROUND: In a previous study, shaking speed was found to be an important factor affecting the population dynamics and lignocellulose-degrading activities of a synthetic lignocellulolytic microbial consortium composed of the bacteria Sphingobacterium paramultivorum w15, Citrobacter freundii so4, a...

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Autores principales: Wang, Yanfang, Jiménez, Diego Javier, Zhang, Zhenhua, van Elsas, Jan Dirk
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10061750/
https://www.ncbi.nlm.nih.gov/pubmed/36991472
http://dx.doi.org/10.1186/s13068-023-02289-0
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author Wang, Yanfang
Jiménez, Diego Javier
Zhang, Zhenhua
van Elsas, Jan Dirk
author_facet Wang, Yanfang
Jiménez, Diego Javier
Zhang, Zhenhua
van Elsas, Jan Dirk
author_sort Wang, Yanfang
collection PubMed
description BACKGROUND: In a previous study, shaking speed was found to be an important factor affecting the population dynamics and lignocellulose-degrading activities of a synthetic lignocellulolytic microbial consortium composed of the bacteria Sphingobacterium paramultivorum w15, Citrobacter freundii so4, and the fungus Coniochaeta sp. 2T2.1. Here, the gene expression profiles of each strain in this consortium were examined after growth at two shaking speeds (180 and 60 rpm) at three time points (1, 5 and 13 days). RESULTS: The results indicated that, at 60 rpm, C. freundii so4 switched, to a large extent, from aerobic to flexible (aerobic/microaerophilic/anaerobic) metabolism, resulting in continued slow growth till late stage. In addition, Coniochaeta sp. 2T2.1 tended to occur to a larger extent in the hyphal form, with genes encoding adhesion proteins being highly expressed. Much like at 180 rpm, at 60 rpm, S. paramultivorum w15 and Coniochaeta sp. 2T2.1 were key players in hemicellulose degradation processes, as evidenced from the respective CAZy-specific transcripts. Coniochaeta sp. 2T2.1 exhibited expression of genes encoding arabinoxylan-degrading enzymes (i.e., of CAZy groups GH10, GH11, CE1, CE5 and GH43), whereas, at 180 rpm, some of these genes were suppressed at early stages of growth. Moreover, C. freundii so4 stably expressed genes that were predicted to encode proteins with (1) β-xylosidase/β-glucosidase and (2) peptidoglycan/chitinase activities, (3) stress response- and detoxification-related proteins. Finally, S. paramultivorum w15 showed involvement in vitamin B2 generation in the early stages across the two shaking speeds, while this role was taken over by C. freundii so4 at late stage at 60 rpm. CONCLUSIONS: We provide evidence that S. paramultivorum w15 is involved in the degradation of mainly hemicellulose and in vitamin B2 production, and C. freundii so4 in the degradation of oligosaccharides or sugar dimers, next to detoxification processes. Coniochaeta sp. 2T2.1 was held to be strongly involved in cellulose and xylan (at early stages), next to lignin modification processes (at later stages). The synergism and alternative functional roles presented in this study enhance the eco-enzymological understanding of the degradation of lignocellulose in this tripartite microbial consortium. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02289-0.
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spelling pubmed-100617502023-03-31 Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study Wang, Yanfang Jiménez, Diego Javier Zhang, Zhenhua van Elsas, Jan Dirk Biotechnol Biofuels Bioprod Research BACKGROUND: In a previous study, shaking speed was found to be an important factor affecting the population dynamics and lignocellulose-degrading activities of a synthetic lignocellulolytic microbial consortium composed of the bacteria Sphingobacterium paramultivorum w15, Citrobacter freundii so4, and the fungus Coniochaeta sp. 2T2.1. Here, the gene expression profiles of each strain in this consortium were examined after growth at two shaking speeds (180 and 60 rpm) at three time points (1, 5 and 13 days). RESULTS: The results indicated that, at 60 rpm, C. freundii so4 switched, to a large extent, from aerobic to flexible (aerobic/microaerophilic/anaerobic) metabolism, resulting in continued slow growth till late stage. In addition, Coniochaeta sp. 2T2.1 tended to occur to a larger extent in the hyphal form, with genes encoding adhesion proteins being highly expressed. Much like at 180 rpm, at 60 rpm, S. paramultivorum w15 and Coniochaeta sp. 2T2.1 were key players in hemicellulose degradation processes, as evidenced from the respective CAZy-specific transcripts. Coniochaeta sp. 2T2.1 exhibited expression of genes encoding arabinoxylan-degrading enzymes (i.e., of CAZy groups GH10, GH11, CE1, CE5 and GH43), whereas, at 180 rpm, some of these genes were suppressed at early stages of growth. Moreover, C. freundii so4 stably expressed genes that were predicted to encode proteins with (1) β-xylosidase/β-glucosidase and (2) peptidoglycan/chitinase activities, (3) stress response- and detoxification-related proteins. Finally, S. paramultivorum w15 showed involvement in vitamin B2 generation in the early stages across the two shaking speeds, while this role was taken over by C. freundii so4 at late stage at 60 rpm. CONCLUSIONS: We provide evidence that S. paramultivorum w15 is involved in the degradation of mainly hemicellulose and in vitamin B2 production, and C. freundii so4 in the degradation of oligosaccharides or sugar dimers, next to detoxification processes. Coniochaeta sp. 2T2.1 was held to be strongly involved in cellulose and xylan (at early stages), next to lignin modification processes (at later stages). The synergism and alternative functional roles presented in this study enhance the eco-enzymological understanding of the degradation of lignocellulose in this tripartite microbial consortium. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02289-0. BioMed Central 2023-03-29 /pmc/articles/PMC10061750/ /pubmed/36991472 http://dx.doi.org/10.1186/s13068-023-02289-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Wang, Yanfang
Jiménez, Diego Javier
Zhang, Zhenhua
van Elsas, Jan Dirk
Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
title Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
title_full Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
title_fullStr Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
title_full_unstemmed Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
title_short Functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
title_sort functioning of a tripartite lignocellulolytic microbial consortium cultivated under two shaking conditions: a metatranscriptomic study
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10061750/
https://www.ncbi.nlm.nih.gov/pubmed/36991472
http://dx.doi.org/10.1186/s13068-023-02289-0
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