Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite

Detalhes bibliográficos
Autor(a) principal: Moreira, Edimar A.
Data de Publicação: 2021
Outros Autores: Persinoti, Gabriela F., Menezes, Letícia R., Paixão, Douglas A. A., Alvarez, Thabata M., Cairo, João P. L. Franco, Squina, Fabio M., Costa-Leonardo, Ana Maria [UNESP], Rodrigues, Andre [UNESP], Sillam-Dussès, David, Arab, Alberto
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.3389/fevo.2021.632590
http://hdl.handle.net/11449/207717
Resumo: Lignocellulose digestion in termites is achieved through the functional synergy between gut symbionts and host enzymes. However, some species have evolved additional associations with nest microorganisms that collaborate in the decomposition of plant biomass. In a previous study, we determined that plant material packed with feces inside the nests of Cornitermes cumulans (Syntermitinae) harbors a distinct microbial assemblage. These food nodules also showed a high hemicellulolytic activity, possibly acting as an external place for complementary lignocellulose digestion. In this study, we used a combination of ITS sequence analysis, metagenomics, and metatranscriptomics to investigate the presence and differential expression of genes coding for carbohydrate-active enzymes (CAZy) in the food nodules and the gut of workers and soldiers. Our results confirm that food nodules express a distinct set of CAZy genes suggesting that stored plant material is initially decomposed by enzymes that target the lignin and complex polysaccharides from fungi and bacteria before the passage through the gut, where it is further targeted by a complementary set of cellulases, xylanases, and esterases produced by the gut microbiota and the termite host. We also showed that the expression of CAZy transcripts associated to endoglucanases and xylanases was higher in the gut of termites than in the food nodules. An additional finding in this study was the presence of fungi in the termite gut that expressed CAZy genes. This study highlights the importance of externalization of digestion by nest microbes and provides new evidence of complementary digestion in the context of higher termite evolution.
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spelling Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher TermiteBlattodeacarbohydrate active enzymesfood storageIsopteranest microrganismsnutritionsaprotrophsSyntermitinaeLignocellulose digestion in termites is achieved through the functional synergy between gut symbionts and host enzymes. However, some species have evolved additional associations with nest microorganisms that collaborate in the decomposition of plant biomass. In a previous study, we determined that plant material packed with feces inside the nests of Cornitermes cumulans (Syntermitinae) harbors a distinct microbial assemblage. These food nodules also showed a high hemicellulolytic activity, possibly acting as an external place for complementary lignocellulose digestion. In this study, we used a combination of ITS sequence analysis, metagenomics, and metatranscriptomics to investigate the presence and differential expression of genes coding for carbohydrate-active enzymes (CAZy) in the food nodules and the gut of workers and soldiers. Our results confirm that food nodules express a distinct set of CAZy genes suggesting that stored plant material is initially decomposed by enzymes that target the lignin and complex polysaccharides from fungi and bacteria before the passage through the gut, where it is further targeted by a complementary set of cellulases, xylanases, and esterases produced by the gut microbiota and the termite host. We also showed that the expression of CAZy transcripts associated to endoglucanases and xylanases was higher in the gut of termites than in the food nodules. An additional finding in this study was the presence of fungi in the termite gut that expressed CAZy genes. This study highlights the importance of externalization of digestion by nest microbes and provides new evidence of complementary digestion in the context of higher termite evolution.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Centro de Ciências Naturais e Humanas Universidade Federal do ABC (UFABC)Laboratório Nacional de Biorrenováveis (LNBR) Centro Nacional de Pesquisa em Energia e Materiais (CNPEM)Graduate Programme in Industrial Biotechnology Universidade PositivoDepartment of Biochemistry and Tissue Biology Institute of Biology University of CampinasPrograma em Processos Tecnológicos e Ambientais Universidade de Sorocaba (UNISO)Departamento de Biologia Geral e Aplicada Instituto de Biociências Universidade Estadual Paulista (UNESP)Center for the Study of Social Insects São Paulo State University (UNESP)Laboratory of Experimental and Comparative Ethology UR 4443 University Sorbonne Paris NordDepartamento de Biologia Geral e Aplicada Instituto de Biociências Universidade Estadual Paulista (UNESP)Center for the Study of Social Insects São Paulo State University (UNESP)FAPESP: 2015/21497-6FAPESP: 2018/22839-6Universidade Federal do ABC (UFABC)Centro Nacional de Pesquisa em Energia e Materiais (CNPEM)Universidade PositivoUniversidade Estadual de Campinas (UNICAMP)Universidade de Sorocaba (UNISO)Universidade Estadual Paulista (Unesp)University Sorbonne Paris NordMoreira, Edimar A.Persinoti, Gabriela F.Menezes, Letícia R.Paixão, Douglas A. A.Alvarez, Thabata M.Cairo, João P. L. FrancoSquina, Fabio M.Costa-Leonardo, Ana Maria [UNESP]Rodrigues, Andre [UNESP]Sillam-Dussès, DavidArab, Alberto2021-06-25T10:59:50Z2021-06-25T10:59:50Z2021-04-26info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.3389/fevo.2021.632590Frontiers in Ecology and Evolution, v. 9.2296-701Xhttp://hdl.handle.net/11449/20771710.3389/fevo.2021.6325902-s2.0-85105589869Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengFrontiers in Ecology and Evolutioninfo:eu-repo/semantics/openAccess2024-04-11T14:57:20Zoai:repositorio.unesp.br:11449/207717Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T19:48:45.417770Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
title Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
spellingShingle Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
Moreira, Edimar A.
Blattodea
carbohydrate active enzymes
food storage
Isoptera
nest microrganisms
nutrition
saprotrophs
Syntermitinae
title_short Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
title_full Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
title_fullStr Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
title_full_unstemmed Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
title_sort Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
author Moreira, Edimar A.
author_facet Moreira, Edimar A.
Persinoti, Gabriela F.
Menezes, Letícia R.
Paixão, Douglas A. A.
Alvarez, Thabata M.
Cairo, João P. L. Franco
Squina, Fabio M.
Costa-Leonardo, Ana Maria [UNESP]
Rodrigues, Andre [UNESP]
Sillam-Dussès, David
Arab, Alberto
author_role author
author2 Persinoti, Gabriela F.
Menezes, Letícia R.
Paixão, Douglas A. A.
Alvarez, Thabata M.
Cairo, João P. L. Franco
Squina, Fabio M.
Costa-Leonardo, Ana Maria [UNESP]
Rodrigues, Andre [UNESP]
Sillam-Dussès, David
Arab, Alberto
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Federal do ABC (UFABC)
Centro Nacional de Pesquisa em Energia e Materiais (CNPEM)
Universidade Positivo
Universidade Estadual de Campinas (UNICAMP)
Universidade de Sorocaba (UNISO)
Universidade Estadual Paulista (Unesp)
University Sorbonne Paris Nord
dc.contributor.author.fl_str_mv Moreira, Edimar A.
Persinoti, Gabriela F.
Menezes, Letícia R.
Paixão, Douglas A. A.
Alvarez, Thabata M.
Cairo, João P. L. Franco
Squina, Fabio M.
Costa-Leonardo, Ana Maria [UNESP]
Rodrigues, Andre [UNESP]
Sillam-Dussès, David
Arab, Alberto
dc.subject.por.fl_str_mv Blattodea
carbohydrate active enzymes
food storage
Isoptera
nest microrganisms
nutrition
saprotrophs
Syntermitinae
topic Blattodea
carbohydrate active enzymes
food storage
Isoptera
nest microrganisms
nutrition
saprotrophs
Syntermitinae
description Lignocellulose digestion in termites is achieved through the functional synergy between gut symbionts and host enzymes. However, some species have evolved additional associations with nest microorganisms that collaborate in the decomposition of plant biomass. In a previous study, we determined that plant material packed with feces inside the nests of Cornitermes cumulans (Syntermitinae) harbors a distinct microbial assemblage. These food nodules also showed a high hemicellulolytic activity, possibly acting as an external place for complementary lignocellulose digestion. In this study, we used a combination of ITS sequence analysis, metagenomics, and metatranscriptomics to investigate the presence and differential expression of genes coding for carbohydrate-active enzymes (CAZy) in the food nodules and the gut of workers and soldiers. Our results confirm that food nodules express a distinct set of CAZy genes suggesting that stored plant material is initially decomposed by enzymes that target the lignin and complex polysaccharides from fungi and bacteria before the passage through the gut, where it is further targeted by a complementary set of cellulases, xylanases, and esterases produced by the gut microbiota and the termite host. We also showed that the expression of CAZy transcripts associated to endoglucanases and xylanases was higher in the gut of termites than in the food nodules. An additional finding in this study was the presence of fungi in the termite gut that expressed CAZy genes. This study highlights the importance of externalization of digestion by nest microbes and provides new evidence of complementary digestion in the context of higher termite evolution.
publishDate 2021
dc.date.none.fl_str_mv 2021-06-25T10:59:50Z
2021-06-25T10:59:50Z
2021-04-26
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.3389/fevo.2021.632590
Frontiers in Ecology and Evolution, v. 9.
2296-701X
http://hdl.handle.net/11449/207717
10.3389/fevo.2021.632590
2-s2.0-85105589869
url http://dx.doi.org/10.3389/fevo.2021.632590
http://hdl.handle.net/11449/207717
identifier_str_mv Frontiers in Ecology and Evolution, v. 9.
2296-701X
10.3389/fevo.2021.632590
2-s2.0-85105589869
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Frontiers in Ecology and Evolution
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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