Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species

Mesophilic, anaerobic, and cellulolytic Ruminiclostridium-type bacterial species can secrete an extracellular, multi-enzyme machinery cellulosome, which efficiently degrades cellulose. In this study, we first reported the complete genome of Ruminiclostridium papyrosolvens DSM2782, a single circular...

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Main Authors: Mengcheng You, Qiuyun Zhao, Yuansheng Liu, Wenhao Zhang, Zhewei Shen, Zhenxing Ren, Chenggang Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1288286/full
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author Mengcheng You
Mengcheng You
Qiuyun Zhao
Yuansheng Liu
Yuansheng Liu
Wenhao Zhang
Wenhao Zhang
Zhewei Shen
Zhenxing Ren
Chenggang Xu
author_facet Mengcheng You
Mengcheng You
Qiuyun Zhao
Yuansheng Liu
Yuansheng Liu
Wenhao Zhang
Wenhao Zhang
Zhewei Shen
Zhenxing Ren
Chenggang Xu
author_sort Mengcheng You
collection DOAJ
description Mesophilic, anaerobic, and cellulolytic Ruminiclostridium-type bacterial species can secrete an extracellular, multi-enzyme machinery cellulosome, which efficiently degrades cellulose. In this study, we first reported the complete genome of Ruminiclostridium papyrosolvens DSM2782, a single circular 5,027,861-bp chromosome with 37.1% G + C content, and compared it with other Ruminiclostridium-type species. Pan-genome analysis showed that Ruminiclostridium-type species share a large number of core genes to conserve basic functions, although they have a high level of intraspecific genetic diversity. Especially, KEGG mapping revealed that Ruminiclostridium-type species mainly use ABC transporters regulated by two-component systems (TCSs) to absorb extracellular sugars but not phosphotransferase systems (PTSs) that are employed by solventogenic clostridia, such as Clostridium acetobutylicum. Furthermore, we performed comparative analyses of the species-specific repertoire of CAZymes for each of the Ruminiclostridium-type species. The high similarity of their cohesins suggests a common ancestor and potential cross-species recognition. Additionally, both differences between the C-terminal cohesins and other cohesins of scaffoldins and between the dockerins linking with cellulases and other catalytic domains indicate a preference for the location of cellulosomal catalytic subunits at scaffoldins. The information gained in this study may be utilized directly or developed further by genetic engineering and optimizing enzyme systems or cell factories for enhanced biotechnological biomass deconstruction and biofuel production.
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spelling doaj.art-141e6a36a87a4330a4efbc05b23e95542023-11-23T11:13:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-11-011410.3389/fmicb.2023.12882861288286Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type speciesMengcheng You0Mengcheng You1Qiuyun Zhao2Yuansheng Liu3Yuansheng Liu4Wenhao Zhang5Wenhao Zhang6Zhewei Shen7Zhenxing Ren8Chenggang Xu9Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Biotechnology, Shanxi University, Taiyuan, Shanxi Province, ChinaCollege of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang Province, ChinaCollege of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang Province, ChinaKey Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Biotechnology, Shanxi University, Taiyuan, Shanxi Province, ChinaCollege of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang Province, ChinaKey Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Biotechnology, Shanxi University, Taiyuan, Shanxi Province, ChinaCollege of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang Province, ChinaKey Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Biotechnology, Shanxi University, Taiyuan, Shanxi Province, ChinaInstitute of Applied Chemistry, Shanxi University, Taiyuan, Shanxi Province, ChinaCollege of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang Province, ChinaMesophilic, anaerobic, and cellulolytic Ruminiclostridium-type bacterial species can secrete an extracellular, multi-enzyme machinery cellulosome, which efficiently degrades cellulose. In this study, we first reported the complete genome of Ruminiclostridium papyrosolvens DSM2782, a single circular 5,027,861-bp chromosome with 37.1% G + C content, and compared it with other Ruminiclostridium-type species. Pan-genome analysis showed that Ruminiclostridium-type species share a large number of core genes to conserve basic functions, although they have a high level of intraspecific genetic diversity. Especially, KEGG mapping revealed that Ruminiclostridium-type species mainly use ABC transporters regulated by two-component systems (TCSs) to absorb extracellular sugars but not phosphotransferase systems (PTSs) that are employed by solventogenic clostridia, such as Clostridium acetobutylicum. Furthermore, we performed comparative analyses of the species-specific repertoire of CAZymes for each of the Ruminiclostridium-type species. The high similarity of their cohesins suggests a common ancestor and potential cross-species recognition. Additionally, both differences between the C-terminal cohesins and other cohesins of scaffoldins and between the dockerins linking with cellulases and other catalytic domains indicate a preference for the location of cellulosomal catalytic subunits at scaffoldins. The information gained in this study may be utilized directly or developed further by genetic engineering and optimizing enzyme systems or cell factories for enhanced biotechnological biomass deconstruction and biofuel production.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1288286/fullRuminiclostridium papyrosolvenscomparative genomicspan-genomeCAZymescellulosome
spellingShingle Mengcheng You
Mengcheng You
Qiuyun Zhao
Yuansheng Liu
Yuansheng Liu
Wenhao Zhang
Wenhao Zhang
Zhewei Shen
Zhenxing Ren
Chenggang Xu
Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species
Frontiers in Microbiology
Ruminiclostridium papyrosolvens
comparative genomics
pan-genome
CAZymes
cellulosome
title Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species
title_full Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species
title_fullStr Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species
title_full_unstemmed Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species
title_short Insights into lignocellulose degradation: comparative genomics of anaerobic and cellulolytic Ruminiclostridium-type species
title_sort insights into lignocellulose degradation comparative genomics of anaerobic and cellulolytic ruminiclostridium type species
topic Ruminiclostridium papyrosolvens
comparative genomics
pan-genome
CAZymes
cellulosome
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1288286/full
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