Phylogenomics reveals that asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene

Detalhes bibliográficos
Autor(a) principal: Comandatore, Francesco
Data de Publicação: 2021
Outros Autores: 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
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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spelling 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)
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