Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene
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/10.1128/mBio.00106-21 http://hdl.handle.net/11449/208545 |
Resumo: | The mosquito microbiota is composed of several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given their abundance in the gut, reproductive organs, and salivary glands of different mosquito species, while their presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly), Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia expe-rienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result high-lights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants. IMPORTANCE We have studied genome reduction within several strains of the insect symbiont Asaia isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyreth-roid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector Anopheles darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining resistance to insecticides. |
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Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading geneAsaiaGenome reductionPyrethroid hydrolaseThe mosquito microbiota is composed of several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given their abundance in the gut, reproductive organs, and salivary glands of different mosquito species, while their presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly), Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia expe-rienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result high-lights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants. IMPORTANCE We have studied genome reduction within several strains of the insect symbiont Asaia isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyreth-roid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector Anopheles darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining resistance to insecticides.Università degli Studi di CamerinoMinistero dell’Istruzione, dell’Università e della RicercaPediatric CRC Romeo ed Enrica Invernizzi Department of Biosciences Università di MilanoSchool of Biosciences & Veterinary Medicine University of CamerinoCIRM Italian Malaria Network Unit of CamerinoBiotechnology Institute (IBTEC) Sao Paulo State University (UNESP)Biosciences Institute at Botucatu (IBB) Sao Paulo State University (UNESP)Department of Biology and Biotechnology University of PaviaIstituto Zooprofilattico Sperimentale delle VenezieMRC-University of Glasgow Centre for Virus ResearchPediatric CRC Romeo ed Enrica Invernizzi DIBIC Università di MilanoBiotechnology Institute (IBTEC) Sao Paulo State University (UNESP)Biosciences Institute at Botucatu (IBB) Sao Paulo State University (UNESP)Ministero dell’Istruzione, dell’Università e della Ricerca: 2017J8JR57Ministero dell’Istruzione, dell’Università e della Ricerca: FAR2019Università di MilanoUniversity of CamerinoUnit of CamerinoUniversidade Estadual Paulista (Unesp)University of PaviaIstituto Zooprofilattico Sperimentale delle VenezieMRC-University of Glasgow Centre for Virus ResearchComandatore, FrancescoDamiani, ClaudiaCappelli, AlessiaRibolla, Paulo Eduardo Martins [UNESP]Gasperi, GiulianoGradoni, FrancescoCapelli, GioiaPiazza, AuroraMontarsi, FabrizioMancini, Maria VittoriaRossi, PaoloRicci, IreneBandi, ClaudioFavia, Guido2021-06-25T11:13:48Z2021-06-25T11:13:48Z2021-01-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1128/mBio.00106-21mBio, v. 12, n. 2, 2021.2150-75112161-2129http://hdl.handle.net/11449/20854510.1128/mBio.00106-212-s2.0-85103290045Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengmBioinfo:eu-repo/semantics/openAccess2021-10-23T19:02:14Zoai:repositorio.unesp.br:11449/208545Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T17:54:26.187033Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
title |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
spellingShingle |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene Comandatore, Francesco Asaia Genome reduction Pyrethroid hydrolase |
title_short |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
title_full |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
title_fullStr |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
title_full_unstemmed |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
title_sort |
Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene |
author |
Comandatore, Francesco |
author_facet |
Comandatore, Francesco Damiani, Claudia Cappelli, Alessia Ribolla, Paulo Eduardo Martins [UNESP] Gasperi, Giuliano Gradoni, Francesco Capelli, Gioia Piazza, Aurora Montarsi, Fabrizio Mancini, Maria Vittoria Rossi, Paolo Ricci, Irene Bandi, Claudio Favia, Guido |
author_role |
author |
author2 |
Damiani, Claudia Cappelli, Alessia Ribolla, Paulo Eduardo Martins [UNESP] Gasperi, Giuliano Gradoni, Francesco Capelli, Gioia Piazza, Aurora Montarsi, Fabrizio Mancini, Maria Vittoria Rossi, Paolo Ricci, Irene Bandi, Claudio Favia, Guido |
author2_role |
author author author author author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Università di Milano University of Camerino Unit of Camerino Universidade Estadual Paulista (Unesp) University of Pavia Istituto Zooprofilattico Sperimentale delle Venezie MRC-University of Glasgow Centre for Virus Research |
dc.contributor.author.fl_str_mv |
Comandatore, Francesco Damiani, Claudia Cappelli, Alessia Ribolla, Paulo Eduardo Martins [UNESP] Gasperi, Giuliano Gradoni, Francesco Capelli, Gioia Piazza, Aurora Montarsi, Fabrizio Mancini, Maria Vittoria Rossi, Paolo Ricci, Irene Bandi, Claudio Favia, Guido |
dc.subject.por.fl_str_mv |
Asaia Genome reduction Pyrethroid hydrolase |
topic |
Asaia Genome reduction Pyrethroid hydrolase |
description |
The mosquito microbiota is composed of several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given their abundance in the gut, reproductive organs, and salivary glands of different mosquito species, while their presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly), Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia expe-rienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result high-lights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants. IMPORTANCE We have studied genome reduction within several strains of the insect symbiont Asaia isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyreth-roid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector Anopheles darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining resistance to insecticides. |
publishDate |
2021 |
dc.date.none.fl_str_mv |
2021-06-25T11:13:48Z 2021-06-25T11:13:48Z 2021-01-01 |
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/10.1128/mBio.00106-21 mBio, v. 12, n. 2, 2021. 2150-7511 2161-2129 http://hdl.handle.net/11449/208545 10.1128/mBio.00106-21 2-s2.0-85103290045 |
url |
http://dx.doi.org/10.1128/mBio.00106-21 http://hdl.handle.net/11449/208545 |
identifier_str_mv |
mBio, v. 12, n. 2, 2021. 2150-7511 2161-2129 10.1128/mBio.00106-21 2-s2.0-85103290045 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
mBio |
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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1808128874153771008 |