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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1179206/full |
| _version_ | 1797813755236581376 |
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| author | Renaud Berlemont |
| author_facet | Renaud Berlemont |
| author_sort | Renaud Berlemont |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-13T07:56:29Z |
| format | Article |
| id | doaj.art-c72ce0900c174e9785c6a5cb12bc5e9e |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-13T07:56:29Z |
| publishDate | 2023-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-c72ce0900c174e9785c6a5cb12bc5e9e2023-06-02T04:39:12ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-06-011410.3389/fmicb.2023.11792061179206The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteriaRenaud BerlemontGlycoside 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.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1179206/fullglycoside hydrolasecellulaseCAZygenomicspolysaccharide utilizationgene cluster |
| spellingShingle | Renaud Berlemont The supragenic organization of glycoside hydrolase encoding genes reveals distinct strategies for carbohydrate utilization in bacteria Frontiers in Microbiology glycoside hydrolase cellulase CAZy genomics polysaccharide utilization gene cluster |
| 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 | glycoside hydrolase cellulase CAZy genomics polysaccharide utilization gene cluster |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1179206/full |
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