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Unveiling lignocellulolytic potential: a genomic exploration of bacterial lineages within the termite gut

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Title: Unveiling lignocellulolytic potential: a genomic exploration of bacterial lineages within the termite gut
Authors: Salgado, João Felipe M., Hervé, Vincent, Vera, Manuel, Tokuda, Gaku, Brune, Andreas
Contributors: Hervé, Vincent, Research Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, Marburg, Tropical Biosphere Research Center, Center of Molecular Biosciences, University of the Ryukyus, Nishihara, Okinawa
Source: Microbiome
Microbiome, Vol 12, Iss 1, Pp 1-16 (2024)
Microbiome, 12(1):201
Publisher Information: Springer Science and Business Media LLC, 2024.
Publication Year: 2024
Subject Terms: Bacteria, Research, QR100-130, Functional genomics, Isoptera, Genomics, Lignin, Gastrointestinal Microbiome, [SDE.BE] Environmental Sciences/Biodiversity and Ecology, Microbial ecology, Cellulase, Polysaccharides, Lignocellulose degradation, Animals, Metagenome, Genome, Bacterial [MeSH], Bacteria/genetics [MeSH], Gastrointestinal Microbiome [MeSH], Animals [MeSH], Phylogeny [MeSH], Metagenome [MeSH], Termite microbiota, Lignin/metabolism [MeSH], Cellulose/metabolism [MeSH], Bacteria/enzymology [MeSH], Genomics [MeSH], Bacteria/classification [MeSH], CAZymes, Polysaccharides/metabolism [MeSH], Bacteria/isolation, Isoptera/microbiology [MeSH], [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Cellulose, Phylogeny, Genome, Bacterial
Description: Background The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT. Results We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall. Conclusions The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT.
Document Type: Article
Other literature type
File Description: application/pdf
Language: English
ISSN: 2049-2618
DOI: 10.1186/s40168-024-01917-7
Access URL: https://pubmed.ncbi.nlm.nih.gov/39407345
https://doaj.org/article/6505f9139e3e47a0bbf3aeb08e4c70dc
https://repository.publisso.de/resource/frl:6509063
Rights: CC BY
Accession Number: edsair.doi.dedup.....afdca50ca5d6792caefe595aa02f06bb
Database: OpenAIRE
Description
Abstract:Background The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT. Results We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall. Conclusions The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT.
ISSN:20492618
DOI:10.1186/s40168-024-01917-7