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Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites

BACKGROUND: Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. They mainly feed on wood and other plant material at different stages of humification. Lignocellulose is often a principal component of such plant diet, and...

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Autores principales: Marynowska, Martyna, Goux, Xavier, Sillam-Dussès, David, Rouland-Lefèvre, Corinne, Halder, Rashi, Wilmes, Paul, Gawron, Piotr, Roisin, Yves, Delfosse, Philippe, Calusinska, Magdalena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7313118/
https://www.ncbi.nlm.nih.gov/pubmed/32576253
http://dx.doi.org/10.1186/s40168-020-00872-3
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author Marynowska, Martyna
Goux, Xavier
Sillam-Dussès, David
Rouland-Lefèvre, Corinne
Halder, Rashi
Wilmes, Paul
Gawron, Piotr
Roisin, Yves
Delfosse, Philippe
Calusinska, Magdalena
author_facet Marynowska, Martyna
Goux, Xavier
Sillam-Dussès, David
Rouland-Lefèvre, Corinne
Halder, Rashi
Wilmes, Paul
Gawron, Piotr
Roisin, Yves
Delfosse, Philippe
Calusinska, Magdalena
author_sort Marynowska, Martyna
collection PubMed
description BACKGROUND: Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. They mainly feed on wood and other plant material at different stages of humification. Lignocellulose is often a principal component of such plant diet, and termites largely rely on their symbiotic microbiota and associated enzymes to decompose their food efficiently. While lower termites and their gut flagellates were given larger scientific attention in the past, the gut lignocellulolytic bacteria of higher termites remain less explored. Therefore, in this study, we investigated the structure and function of gut prokaryotic microbiomes from 11 higher termite genera representative of Syntermitinae, Apicotermitinae, Termitidae and Nasutitermitinae subfamilies, broadly grouped into plant fibre- and soil-feeding termite categories. RESULTS: Despite the different compositional structures of the studied termite gut microbiomes, reflecting well the diet and host lineage, we observed a surprisingly high functional congruency between gut metatranscriptomes from both feeding groups. The abundance of transcripts encoding for carbohydrate active enzymes as well as expression and diversity profiles of assigned glycoside hydrolase families were also similar between plant fibre- and soil-feeding termites. Yet, dietary imprints highlighted subtle metabolic differences specific to each feeding category. Roughly, 0.18% of de novo re-constructed gene transcripts were shared between the different termite gut microbiomes, making each termite gut a unique reservoir of genes encoding for potentially industrially applicable enzymes, e.g. relevant to biomass degradation. Taken together, we demonstrated the functional equivalence in microbial populations across different termite hosts. CONCLUSIONS: Our results provide valuable insight into the bacterial component of the termite gut system and significantly expand the inventory of termite prokaryotic genes participating in the deconstruction of plant biomass.
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spelling pubmed-73131182020-06-24 Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites Marynowska, Martyna Goux, Xavier Sillam-Dussès, David Rouland-Lefèvre, Corinne Halder, Rashi Wilmes, Paul Gawron, Piotr Roisin, Yves Delfosse, Philippe Calusinska, Magdalena Microbiome Research BACKGROUND: Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. They mainly feed on wood and other plant material at different stages of humification. Lignocellulose is often a principal component of such plant diet, and termites largely rely on their symbiotic microbiota and associated enzymes to decompose their food efficiently. While lower termites and their gut flagellates were given larger scientific attention in the past, the gut lignocellulolytic bacteria of higher termites remain less explored. Therefore, in this study, we investigated the structure and function of gut prokaryotic microbiomes from 11 higher termite genera representative of Syntermitinae, Apicotermitinae, Termitidae and Nasutitermitinae subfamilies, broadly grouped into plant fibre- and soil-feeding termite categories. RESULTS: Despite the different compositional structures of the studied termite gut microbiomes, reflecting well the diet and host lineage, we observed a surprisingly high functional congruency between gut metatranscriptomes from both feeding groups. The abundance of transcripts encoding for carbohydrate active enzymes as well as expression and diversity profiles of assigned glycoside hydrolase families were also similar between plant fibre- and soil-feeding termites. Yet, dietary imprints highlighted subtle metabolic differences specific to each feeding category. Roughly, 0.18% of de novo re-constructed gene transcripts were shared between the different termite gut microbiomes, making each termite gut a unique reservoir of genes encoding for potentially industrially applicable enzymes, e.g. relevant to biomass degradation. Taken together, we demonstrated the functional equivalence in microbial populations across different termite hosts. CONCLUSIONS: Our results provide valuable insight into the bacterial component of the termite gut system and significantly expand the inventory of termite prokaryotic genes participating in the deconstruction of plant biomass. BioMed Central 2020-06-23 /pmc/articles/PMC7313118/ /pubmed/32576253 http://dx.doi.org/10.1186/s40168-020-00872-3 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Marynowska, Martyna
Goux, Xavier
Sillam-Dussès, David
Rouland-Lefèvre, Corinne
Halder, Rashi
Wilmes, Paul
Gawron, Piotr
Roisin, Yves
Delfosse, Philippe
Calusinska, Magdalena
Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
title Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
title_full Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
title_fullStr Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
title_full_unstemmed Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
title_short Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
title_sort compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7313118/
https://www.ncbi.nlm.nih.gov/pubmed/32576253
http://dx.doi.org/10.1186/s40168-020-00872-3
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