A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides

Background Lignocellulose is a renewable and enormous biomass resource, which can be degraded efficiently by a range of cocktails of carbohydrate-active enzymes secreted by termite gut symbiotic bacteria. There is an urgent need to find enzymes with novel characteristics for improving the conversion...

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Main Authors: Nguyen Thi-Hanh Vu, Tung Ngoc Quach, Xuan Thi-Thanh Dao, Ha Thanh Le, Chi Phuong Le, Lam Tung Nguyen, Lam Tung Le, Cuong Cao Ngo, Ha Hoang, Ha Hoang Chu, Quyet-Tien Phi
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Language:English
Published: PeerJ Inc. 2021-07-01
Series:PeerJ
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Online Access:https://peerj.com/articles/11839.pdf
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collection DOAJ
language English
format Article
sources DOAJ
author Nguyen Thi-Hanh Vu
Tung Ngoc Quach
Xuan Thi-Thanh Dao
Ha Thanh Le
Chi Phuong Le
Lam Tung Nguyen
Lam Tung Le
Cuong Cao Ngo
Ha Hoang
Ha Hoang Chu
Quyet-Tien Phi
spellingShingle Nguyen Thi-Hanh Vu
Tung Ngoc Quach
Xuan Thi-Thanh Dao
Ha Thanh Le
Chi Phuong Le
Lam Tung Nguyen
Lam Tung Le
Cuong Cao Ngo
Ha Hoang
Ha Hoang Chu
Quyet-Tien Phi
A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides
PeerJ
Carbohydrate-active enzymes
Cellulosimicrobium cellulans
Levan
Lignocellulose
Termite guts
Whole-genome sequencing
author_facet Nguyen Thi-Hanh Vu
Tung Ngoc Quach
Xuan Thi-Thanh Dao
Ha Thanh Le
Chi Phuong Le
Lam Tung Nguyen
Lam Tung Le
Cuong Cao Ngo
Ha Hoang
Ha Hoang Chu
Quyet-Tien Phi
author_sort Nguyen Thi-Hanh Vu
title A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides
title_short A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides
title_full A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides
title_fullStr A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides
title_full_unstemmed A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharides
title_sort genomic perspective on the potential of termite-associated cellulosimicrobium cellulans mp1 as producer of plant biomass-acting enzymes and exopolysaccharides
publisher PeerJ Inc.
series PeerJ
issn 2167-8359
publishDate 2021-07-01
description Background Lignocellulose is a renewable and enormous biomass resource, which can be degraded efficiently by a range of cocktails of carbohydrate-active enzymes secreted by termite gut symbiotic bacteria. There is an urgent need to find enzymes with novel characteristics for improving the conversion processes in the production of lignocellulosic-based products. Although various studies dedicated to the genus Cellulosimicrobium as gut symbiont, genetic potential related to plant biomass-acting enzymes and exopolysaccharides production has been fully untapped to date. Methods The cellulolytic bacterial strain MP1 was isolated from termite guts and identified to the species level by phenotypic, phylogenetic, and genomic analysis. To further explore genes related to cellulose and hemicellulose degradation, the draft genome of strain MP1 was obtained by using whole-genome sequencing, assembly, and annotation through the Illumina platform. Lignocellulose degrading enzymes and levan production in the liquid medium were also examined to shed light on bacterial activities. Results Among 65 isolates obtained, the strain MP1 was the most efficient cellulase producer with cellulase activity of 0.65 ± 0.02 IU/ml. The whole genome analysis depicted that strain MP1 consists of a circular chromosome that contained 4,580,223 bp with an average GC content of 73.9%. The genome comprises 23 contigs including 67 rRNA genes, three tRNA genes, a single tmRNA gene, and 4,046 protein-coding sequences. In support of the phenotypic identification, the 16S rRNA gene sequence, average nucleotide identity, and whole-genome-based taxonomic analysis demonstrated that the strain MP1 belongs to the species Cellulosimicrobium cellulans. A total of 30 genes related to the degradation of cellulases and hemicellulases were identified in the C. cellulans MP1 genome. Of note, the presence of sacC1-levB-sacC2-ls operon responsible for levan and levan-type fructooligosaccharides biosynthesis was detected in strain MP1 genome, but not with closely related C. cellulans strains, proving this strain to be a potential candidate for further studies. Endoglucanases, exoglucanases, and xylanase were achieved by using cheaply available agro-residues such as rice bran and sugar cane bagasse. The maximum levan production by C. cellulans MP1 was 14.8 ± 1.2 g/l after 20 h of cultivation in media containing 200 g/l sucrose. To the best of our knowledge, the present study is the first genome-based analysis of a Cellulosimicrobium species which focuses on lignocellulosic enzymes and levan biosynthesis, illustrating that the C. cellulans MP1 has a great potential to be an efficient platform for basic research and industrial exploitation.
topic Carbohydrate-active enzymes
Cellulosimicrobium cellulans
Levan
Lignocellulose
Termite guts
Whole-genome sequencing
url https://peerj.com/articles/11839.pdf
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spelling doaj-569af6c4c62e40699b154817e97c97ec2021-07-30T15:05:10ZengPeerJ Inc.PeerJ2167-83592021-07-019e1183910.7717/peerj.11839A genomic perspective on the potential of termite-associated Cellulosimicrobium cellulans MP1 as producer of plant biomass-acting enzymes and exopolysaccharidesNguyen Thi-Hanh Vu0Tung Ngoc Quach1Xuan Thi-Thanh Dao2Ha Thanh Le3Chi Phuong Le4Lam Tung Nguyen5Lam Tung Le6Cuong Cao Ngo7Ha Hoang8Ha Hoang Chu9Quyet-Tien Phi10Institute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamInstitute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamSchool of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, VietnamSchool of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, VietnamInstitute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamSchool of Biotechnology and Food Technology, Hanoi University of Science and Technology, Hanoi, VietnamInstitute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamVietnam–Russia Tropical Center, Hanoi, VietnamInstitute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamInstitute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamInstitute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam, Hanoi, VietnamBackground Lignocellulose is a renewable and enormous biomass resource, which can be degraded efficiently by a range of cocktails of carbohydrate-active enzymes secreted by termite gut symbiotic bacteria. There is an urgent need to find enzymes with novel characteristics for improving the conversion processes in the production of lignocellulosic-based products. Although various studies dedicated to the genus Cellulosimicrobium as gut symbiont, genetic potential related to plant biomass-acting enzymes and exopolysaccharides production has been fully untapped to date. Methods The cellulolytic bacterial strain MP1 was isolated from termite guts and identified to the species level by phenotypic, phylogenetic, and genomic analysis. To further explore genes related to cellulose and hemicellulose degradation, the draft genome of strain MP1 was obtained by using whole-genome sequencing, assembly, and annotation through the Illumina platform. Lignocellulose degrading enzymes and levan production in the liquid medium were also examined to shed light on bacterial activities. Results Among 65 isolates obtained, the strain MP1 was the most efficient cellulase producer with cellulase activity of 0.65 ± 0.02 IU/ml. The whole genome analysis depicted that strain MP1 consists of a circular chromosome that contained 4,580,223 bp with an average GC content of 73.9%. The genome comprises 23 contigs including 67 rRNA genes, three tRNA genes, a single tmRNA gene, and 4,046 protein-coding sequences. In support of the phenotypic identification, the 16S rRNA gene sequence, average nucleotide identity, and whole-genome-based taxonomic analysis demonstrated that the strain MP1 belongs to the species Cellulosimicrobium cellulans. A total of 30 genes related to the degradation of cellulases and hemicellulases were identified in the C. cellulans MP1 genome. Of note, the presence of sacC1-levB-sacC2-ls operon responsible for levan and levan-type fructooligosaccharides biosynthesis was detected in strain MP1 genome, but not with closely related C. cellulans strains, proving this strain to be a potential candidate for further studies. Endoglucanases, exoglucanases, and xylanase were achieved by using cheaply available agro-residues such as rice bran and sugar cane bagasse. The maximum levan production by C. cellulans MP1 was 14.8 ± 1.2 g/l after 20 h of cultivation in media containing 200 g/l sucrose. To the best of our knowledge, the present study is the first genome-based analysis of a Cellulosimicrobium species which focuses on lignocellulosic enzymes and levan biosynthesis, illustrating that the C. cellulans MP1 has a great potential to be an efficient platform for basic research and industrial exploitation.https://peerj.com/articles/11839.pdfCarbohydrate-active enzymesCellulosimicrobium cellulansLevanLignocelluloseTermite gutsWhole-genome sequencing