Complementary Contribution of Fungi and Bacteria to Lignocellulose Digestion in the Food Stored by a Neotropical Higher Termite
Autor(a) principal: | |
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Data de Publicação: | 2021 |
Outros Autores: | , , , , , , , , , |
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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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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_version_ |
1808129120835469312 |