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Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1
Xylan is the most abundant hemicellulose in hardwood and graminaceous plants. It is a heteropolysaccharide comprising different moieties appended to the xylose units. Complete degradation of xylan requires an arsenal of xylanolytic enzymes that can remove the substitutions and mediate internal hydro...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2023
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269863/ https://www.ncbi.nlm.nih.gov/pubmed/37071006 http://dx.doi.org/10.1128/spectrum.05028-22 |
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author | Mukherjee, Saumashish Lodha, Tushar Dilipchand Madhuprakash, Jogi |
author_facet | Mukherjee, Saumashish Lodha, Tushar Dilipchand Madhuprakash, Jogi |
author_sort | Mukherjee, Saumashish |
collection | PubMed |
description | Xylan is the most abundant hemicellulose in hardwood and graminaceous plants. It is a heteropolysaccharide comprising different moieties appended to the xylose units. Complete degradation of xylan requires an arsenal of xylanolytic enzymes that can remove the substitutions and mediate internal hydrolysis of the xylan backbone. Here, we describe the xylan degradation potential and underlying enzyme machinery of the strain, Paenibacillus sp. LS1. The strain LS1 was able to utilize both beechwood and corncob xylan as the sole source of carbon, with the former being the preferred substrate. Genome analysis revealed an extensive xylan-active CAZyme repertoire capable of mediating efficient degradation of the complex polymer. In addition to this, a putative xylooligosaccharide ABC transporter and homologues of the enzymes involved in the xylose isomerase pathway were identified. Further, we have validated the expression of selected xylan-active CAZymes, transporters, and metabolic enzymes during growth of the LS1 on xylan substrates using qRT-PCR. The genome comparison and genomic index (average nucleotide identity [ANI] and digital DNA-DNA hybridization) values revealed that strain LS1 is a novel species of the genus Paenibacillus. Lastly, comparative genome analysis of 238 genomes revealed the prevalence of xylan-active CAZymes over cellulose across the Paenibacillus genus. Taken together, our results indicate that Paenibacillus sp. LS1 is an efficient degrader of xylan polymers, with potential implications in the production of biofuels and other beneficial by-products from lignocellulosic biomass. IMPORTANCE Xylan is the most abundant hemicellulose in the lignocellulosic (plant) biomass that requires cooperative deconstruction by an arsenal of different xylanolytic enzymes to produce xylose and xylooligosaccharides. Microbial (particularly, bacterial) candidates that encode such enzymes are an asset to the biorefineries to mediate efficient and eco-friendly deconstruction of xylan to generate products of value. Although xylan degradation by a few Paenibacillus spp. is reported, a complete genus-wide understanding of the said trait is unavailable till date. Through comparative genome analysis, we showed the prevalence of xylan-active CAZymes across Paenibacillus spp., therefore making them an attractive option towards efficient xylan degradation. Additionally, we deciphered the xylan degradation potential of the strain Paenibacillus sp. LS1 through genome analysis, expression profiling, and biochemical studies. The ability of Paenibacillus sp. LS1 to degrade different xylan types obtained from different plant species, emphasizes its potential implication in lignocellulosic biorefineries. |
format | Online Article Text |
id | pubmed-10269863 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-102698632023-06-16 Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 Mukherjee, Saumashish Lodha, Tushar Dilipchand Madhuprakash, Jogi Microbiol Spectr Research Article Xylan is the most abundant hemicellulose in hardwood and graminaceous plants. It is a heteropolysaccharide comprising different moieties appended to the xylose units. Complete degradation of xylan requires an arsenal of xylanolytic enzymes that can remove the substitutions and mediate internal hydrolysis of the xylan backbone. Here, we describe the xylan degradation potential and underlying enzyme machinery of the strain, Paenibacillus sp. LS1. The strain LS1 was able to utilize both beechwood and corncob xylan as the sole source of carbon, with the former being the preferred substrate. Genome analysis revealed an extensive xylan-active CAZyme repertoire capable of mediating efficient degradation of the complex polymer. In addition to this, a putative xylooligosaccharide ABC transporter and homologues of the enzymes involved in the xylose isomerase pathway were identified. Further, we have validated the expression of selected xylan-active CAZymes, transporters, and metabolic enzymes during growth of the LS1 on xylan substrates using qRT-PCR. The genome comparison and genomic index (average nucleotide identity [ANI] and digital DNA-DNA hybridization) values revealed that strain LS1 is a novel species of the genus Paenibacillus. Lastly, comparative genome analysis of 238 genomes revealed the prevalence of xylan-active CAZymes over cellulose across the Paenibacillus genus. Taken together, our results indicate that Paenibacillus sp. LS1 is an efficient degrader of xylan polymers, with potential implications in the production of biofuels and other beneficial by-products from lignocellulosic biomass. IMPORTANCE Xylan is the most abundant hemicellulose in the lignocellulosic (plant) biomass that requires cooperative deconstruction by an arsenal of different xylanolytic enzymes to produce xylose and xylooligosaccharides. Microbial (particularly, bacterial) candidates that encode such enzymes are an asset to the biorefineries to mediate efficient and eco-friendly deconstruction of xylan to generate products of value. Although xylan degradation by a few Paenibacillus spp. is reported, a complete genus-wide understanding of the said trait is unavailable till date. Through comparative genome analysis, we showed the prevalence of xylan-active CAZymes across Paenibacillus spp., therefore making them an attractive option towards efficient xylan degradation. Additionally, we deciphered the xylan degradation potential of the strain Paenibacillus sp. LS1 through genome analysis, expression profiling, and biochemical studies. The ability of Paenibacillus sp. LS1 to degrade different xylan types obtained from different plant species, emphasizes its potential implication in lignocellulosic biorefineries. American Society for Microbiology 2023-04-18 /pmc/articles/PMC10269863/ /pubmed/37071006 http://dx.doi.org/10.1128/spectrum.05028-22 Text en Copyright © 2023 Mukherjee et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Mukherjee, Saumashish Lodha, Tushar Dilipchand Madhuprakash, Jogi Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 |
title | Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 |
title_full | Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 |
title_fullStr | Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 |
title_full_unstemmed | Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 |
title_short | Comprehensive Genome Analysis of Cellulose and Xylan-Active CAZymes from the Genus Paenibacillus: Special Emphasis on the Novel Xylanolytic Paenibacillus sp. LS1 |
title_sort | comprehensive genome analysis of cellulose and xylan-active cazymes from the genus paenibacillus: special emphasis on the novel xylanolytic paenibacillus sp. ls1 |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269863/ https://www.ncbi.nlm.nih.gov/pubmed/37071006 http://dx.doi.org/10.1128/spectrum.05028-22 |
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