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The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria

Glycoside hydrolases (GHs) are carbohydrate-active enzymes essential for many environmental (e.g., carbon cycling) and biotechnological (e.g., biofuels) processes. The complete processing of carbohydrates by bacteria requires many enzymes acting synergistically. Here, I investigated the clustered or...

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Autor principal: Berlemont, Renaud
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272396/
https://www.ncbi.nlm.nih.gov/pubmed/37333644
http://dx.doi.org/10.3389/fmicb.2023.1179206
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author Berlemont, Renaud
author_facet Berlemont, Renaud
author_sort Berlemont, Renaud
collection PubMed
description Glycoside hydrolases (GHs) are carbohydrate-active enzymes essential for many environmental (e.g., carbon cycling) and biotechnological (e.g., biofuels) processes. The complete processing of carbohydrates by bacteria requires many enzymes acting synergistically. Here, I investigated the clustered or scattered distribution of 406,337 GH-genes and their association with transporter genes identified in 15,640 completely sequenced bacterial genomes. Different bacterial lineages displayed conserved levels of clustered or scattered GH-genes, but overall, the GH-genes clustering was generally higher than in randomized genomes. In lineages with highly clustered GH-genes (e.g., Bacteroides, Paenibacillus), clustered genes shared the same orientation. These codirectional gene clusters potentially facilitate the genes' co-expression by allowing transcriptional read-through and, at least in some cases, forming operons. In several taxa, the GH-genes clustered with distinct types of transporter genes. The type of transporter genes and the distribution of the so-called GH:TR-genes clusters were conserved in selected lineages. Globally, the phylogenetically conserved clustering of the GH-genes with transporter genes highlights the central function of carbohydrate processing across bacterial lineages. In addition, in bacteria with the most identified GH-genes, the genomic adaptations for carbohydrate processing also mirrored the broad environmental origin of the sequenced strains (e.g., soil and mammal gut) suggesting that a combination of evolutionary history and the environment selects for the specific supragenic organization of the GH-genes supporting the carbohydrate processing in bacterial genomes.
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spelling pubmed-102723962023-06-17 The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria Berlemont, Renaud Front Microbiol Microbiology Glycoside hydrolases (GHs) are carbohydrate-active enzymes essential for many environmental (e.g., carbon cycling) and biotechnological (e.g., biofuels) processes. The complete processing of carbohydrates by bacteria requires many enzymes acting synergistically. Here, I investigated the clustered or scattered distribution of 406,337 GH-genes and their association with transporter genes identified in 15,640 completely sequenced bacterial genomes. Different bacterial lineages displayed conserved levels of clustered or scattered GH-genes, but overall, the GH-genes clustering was generally higher than in randomized genomes. In lineages with highly clustered GH-genes (e.g., Bacteroides, Paenibacillus), clustered genes shared the same orientation. These codirectional gene clusters potentially facilitate the genes' co-expression by allowing transcriptional read-through and, at least in some cases, forming operons. In several taxa, the GH-genes clustered with distinct types of transporter genes. The type of transporter genes and the distribution of the so-called GH:TR-genes clusters were conserved in selected lineages. Globally, the phylogenetically conserved clustering of the GH-genes with transporter genes highlights the central function of carbohydrate processing across bacterial lineages. In addition, in bacteria with the most identified GH-genes, the genomic adaptations for carbohydrate processing also mirrored the broad environmental origin of the sequenced strains (e.g., soil and mammal gut) suggesting that a combination of evolutionary history and the environment selects for the specific supragenic organization of the GH-genes supporting the carbohydrate processing in bacterial genomes. Frontiers Media S.A. 2023-06-02 /pmc/articles/PMC10272396/ /pubmed/37333644 http://dx.doi.org/10.3389/fmicb.2023.1179206 Text en Copyright © 2023 Berlemont. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Berlemont, Renaud
The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
title The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
title_full The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
title_fullStr The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
title_full_unstemmed The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
title_short The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
title_sort supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272396/
https://www.ncbi.nlm.nih.gov/pubmed/37333644
http://dx.doi.org/10.3389/fmicb.2023.1179206
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