Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses

Autores
Patané, José S.L.; Martins, Joaquim; Castelão, Ana Beatriz; Nishibe, Christiane; Montera, Luciana; Bigi, Fabiana; Zumárraga, Martín José; Cataldi, Ángel Adrián; Junior, Antônio Fonseca; Roxo, Eliana; Osório, Ana Luiza A. R.; Jorge, Klaudia S.; Thacker, Tyler C.; Almeida, Nalvo F.; Araújo, Flabio R.; Setubal, João C.
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Mycobacterium bovis is an important animal pathogen worldwide, parasitizing wild and domesticated vertebrate live stocks as well as humans. We investigated evolutionary patterns and processes in 38 sequenced genomes of M. bovis from the Americas, Europe, Asia, and Africa. We found that US strains are evolving distinctly (though with low magnitude) from most South American lineages regarding core-coding size, GC-content, and codon usage bias, and we further employ agreement to this pattern as proxy for phylogenetic reliability. Three data types were used for tree inference: 1. Single copy core-coding genes (core-coding); 2. Indel blocks coded as numeric characters (indels); 3. Gene presence/absence similarly coded (pangenome). Core-coding´s performance was below expected regarded we used 2,000+ genes, but indels and pangenome individually estimated reasonable trees, with HGT rates as high as 200x the DNA substitution rate. In addressing why core-coding performed poorly, we excluded phylogenetic method bias, homologous recombination, positive, and purifying selection as possible causes, whilst transient retention of random mildly deleterious mutations due to recent diversification, and also ongoing pseudogeneization, may be plausible. Although total evidence´s retention index was as good as presence/absence data individually in identifying US samples, it additionaly found a South American clade with more lineages excluding only two Brazilian samples. We further inferred divergence times using indels + pangenome due to lack of informativeness of core-coding, recovering relatively similar date estimates to previous studies on the origin of M. bovis (< 10,000 y) regardless of the dating prior (strict vs. uncorrelated clock, uniform vs. exponential clock, different age/rate standard deviation priors), evincing the suitability and unsuspected robustness of using strictly genomic-wide presence/absence data to dating, while also decisively rejecting a strict clock for our dataset. All trees supported a relatively basal position of African strains, which were isolated from Homo sapiens, suggesting it was an important region for early diversification and confirming we were one of the earliest hosts of the species. Evolution of US strains was affected by lateral acquisition of 57 exclusive genes from, including genes important for virulence. A clade of three US localities, distant from one another, is under even faster evolutionary rates supported by core-coding, indels, and pangenome.
Fil: Patané, José S.L.. Universidade de Sao Paulo; Brasil
Fil: Martins, Joaquim. Universidade de Sao Paulo; Brasil
Fil: Castelão, Ana Beatriz. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Nishibe, Christiane. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Montera, Luciana. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Bigi, Fabiana. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Zumárraga, Martín José. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Cataldi, Ángel Adrián. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina
Fil: Junior, Antônio Fonseca. Ministerio da Agricultura Pecuaria e Abastecimento de Brasil. Empresa Brasileira de Pesquisa Agropecuaria; Brasil
Fil: Roxo, Eliana. Instituto Biológico de São Pablo; Brasil
Fil: Osório, Ana Luiza A. R.. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Jorge, Klaudia S.. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Thacker, Tyler C.. United States Department of Agriculture; Estados Unidos
Fil: Almeida, Nalvo F.. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Araújo, Flabio R.. Ministerio da Agricultura Pecuaria e Abastecimento de Brasil. Empresa Brasileira de Pesquisa Agropecuaria; Brasil
Fil: Setubal, João C.. Universidade de Sao Paulo; Brasil. Biocomplexity Institute of Virginia Tech; Estados Unidos
Materia
Mycobacterium
Genome
Bovis
Evolution
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/72516

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spelling Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic AnalysesPatané, José S.L.Martins, JoaquimCastelão, Ana BeatrizNishibe, ChristianeMontera, LucianaBigi, FabianaZumárraga, Martín JoséCataldi, Ángel AdriánJunior, Antônio FonsecaRoxo, ElianaOsório, Ana Luiza A. R.Jorge, Klaudia S.Thacker, Tyler C.Almeida, Nalvo F.Araújo, Flabio R.Setubal, João C.MycobacteriumGenomeBovisEvolutionhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Mycobacterium bovis is an important animal pathogen worldwide, parasitizing wild and domesticated vertebrate live stocks as well as humans. We investigated evolutionary patterns and processes in 38 sequenced genomes of M. bovis from the Americas, Europe, Asia, and Africa. We found that US strains are evolving distinctly (though with low magnitude) from most South American lineages regarding core-coding size, GC-content, and codon usage bias, and we further employ agreement to this pattern as proxy for phylogenetic reliability. Three data types were used for tree inference: 1. Single copy core-coding genes (core-coding); 2. Indel blocks coded as numeric characters (indels); 3. Gene presence/absence similarly coded (pangenome). Core-coding´s performance was below expected regarded we used 2,000+ genes, but indels and pangenome individually estimated reasonable trees, with HGT rates as high as 200x the DNA substitution rate. In addressing why core-coding performed poorly, we excluded phylogenetic method bias, homologous recombination, positive, and purifying selection as possible causes, whilst transient retention of random mildly deleterious mutations due to recent diversification, and also ongoing pseudogeneization, may be plausible. Although total evidence´s retention index was as good as presence/absence data individually in identifying US samples, it additionaly found a South American clade with more lineages excluding only two Brazilian samples. We further inferred divergence times using indels + pangenome due to lack of informativeness of core-coding, recovering relatively similar date estimates to previous studies on the origin of M. bovis (< 10,000 y) regardless of the dating prior (strict vs. uncorrelated clock, uniform vs. exponential clock, different age/rate standard deviation priors), evincing the suitability and unsuspected robustness of using strictly genomic-wide presence/absence data to dating, while also decisively rejecting a strict clock for our dataset. All trees supported a relatively basal position of African strains, which were isolated from Homo sapiens, suggesting it was an important region for early diversification and confirming we were one of the earliest hosts of the species. Evolution of US strains was affected by lateral acquisition of 57 exclusive genes from, including genes important for virulence. A clade of three US localities, distant from one another, is under even faster evolutionary rates supported by core-coding, indels, and pangenome.Fil: Patané, José S.L.. Universidade de Sao Paulo; BrasilFil: Martins, Joaquim. Universidade de Sao Paulo; BrasilFil: Castelão, Ana Beatriz. Universidade Federal do Mato Grosso do Sul; BrasilFil: Nishibe, Christiane. Universidade Federal do Mato Grosso do Sul; BrasilFil: Montera, Luciana. Universidade Federal do Mato Grosso do Sul; BrasilFil: Bigi, Fabiana. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Zumárraga, Martín José. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Cataldi, Ángel Adrián. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; ArgentinaFil: Junior, Antônio Fonseca. Ministerio da Agricultura Pecuaria e Abastecimento de Brasil. Empresa Brasileira de Pesquisa Agropecuaria; BrasilFil: Roxo, Eliana. Instituto Biológico de São Pablo; BrasilFil: Osório, Ana Luiza A. R.. Universidade Federal do Mato Grosso do Sul; BrasilFil: Jorge, Klaudia S.. Universidade Federal do Mato Grosso do Sul; BrasilFil: Thacker, Tyler C.. United States Department of Agriculture; Estados UnidosFil: Almeida, Nalvo F.. Universidade Federal do Mato Grosso do Sul; BrasilFil: Araújo, Flabio R.. Ministerio da Agricultura Pecuaria e Abastecimento de Brasil. Empresa Brasileira de Pesquisa Agropecuaria; BrasilFil: Setubal, João C.. Universidade de Sao Paulo; Brasil. Biocomplexity Institute of Virginia Tech; Estados UnidosOxford University Press2017-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/mswordapplication/pdfhttp://hdl.handle.net/11336/72516Patané, José S.L.; Martins, Joaquim; Castelão, Ana Beatriz; Nishibe, Christiane; Montera, Luciana; et al.; Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses; Oxford University Press; Genome Biology and Evolution; 9; 3; 3-2017; 521-5351759-6653CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/gbe/article/9/3/521/2992613info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evx022info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T15:12:46Zoai:ri.conicet.gov.ar:11336/72516instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 15:12:46.959CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
title Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
spellingShingle Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
Patané, José S.L.
Mycobacterium
Genome
Bovis
Evolution
title_short Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
title_full Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
title_fullStr Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
title_full_unstemmed Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
title_sort Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses
dc.creator.none.fl_str_mv Patané, José S.L.
Martins, Joaquim
Castelão, Ana Beatriz
Nishibe, Christiane
Montera, Luciana
Bigi, Fabiana
Zumárraga, Martín José
Cataldi, Ángel Adrián
Junior, Antônio Fonseca
Roxo, Eliana
Osório, Ana Luiza A. R.
Jorge, Klaudia S.
Thacker, Tyler C.
Almeida, Nalvo F.
Araújo, Flabio R.
Setubal, João C.
author Patané, José S.L.
author_facet Patané, José S.L.
Martins, Joaquim
Castelão, Ana Beatriz
Nishibe, Christiane
Montera, Luciana
Bigi, Fabiana
Zumárraga, Martín José
Cataldi, Ángel Adrián
Junior, Antônio Fonseca
Roxo, Eliana
Osório, Ana Luiza A. R.
Jorge, Klaudia S.
Thacker, Tyler C.
Almeida, Nalvo F.
Araújo, Flabio R.
Setubal, João C.
author_role author
author2 Martins, Joaquim
Castelão, Ana Beatriz
Nishibe, Christiane
Montera, Luciana
Bigi, Fabiana
Zumárraga, Martín José
Cataldi, Ángel Adrián
Junior, Antônio Fonseca
Roxo, Eliana
Osório, Ana Luiza A. R.
Jorge, Klaudia S.
Thacker, Tyler C.
Almeida, Nalvo F.
Araújo, Flabio R.
Setubal, João C.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Mycobacterium
Genome
Bovis
Evolution
topic Mycobacterium
Genome
Bovis
Evolution
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Mycobacterium bovis is an important animal pathogen worldwide, parasitizing wild and domesticated vertebrate live stocks as well as humans. We investigated evolutionary patterns and processes in 38 sequenced genomes of M. bovis from the Americas, Europe, Asia, and Africa. We found that US strains are evolving distinctly (though with low magnitude) from most South American lineages regarding core-coding size, GC-content, and codon usage bias, and we further employ agreement to this pattern as proxy for phylogenetic reliability. Three data types were used for tree inference: 1. Single copy core-coding genes (core-coding); 2. Indel blocks coded as numeric characters (indels); 3. Gene presence/absence similarly coded (pangenome). Core-coding´s performance was below expected regarded we used 2,000+ genes, but indels and pangenome individually estimated reasonable trees, with HGT rates as high as 200x the DNA substitution rate. In addressing why core-coding performed poorly, we excluded phylogenetic method bias, homologous recombination, positive, and purifying selection as possible causes, whilst transient retention of random mildly deleterious mutations due to recent diversification, and also ongoing pseudogeneization, may be plausible. Although total evidence´s retention index was as good as presence/absence data individually in identifying US samples, it additionaly found a South American clade with more lineages excluding only two Brazilian samples. We further inferred divergence times using indels + pangenome due to lack of informativeness of core-coding, recovering relatively similar date estimates to previous studies on the origin of M. bovis (< 10,000 y) regardless of the dating prior (strict vs. uncorrelated clock, uniform vs. exponential clock, different age/rate standard deviation priors), evincing the suitability and unsuspected robustness of using strictly genomic-wide presence/absence data to dating, while also decisively rejecting a strict clock for our dataset. All trees supported a relatively basal position of African strains, which were isolated from Homo sapiens, suggesting it was an important region for early diversification and confirming we were one of the earliest hosts of the species. Evolution of US strains was affected by lateral acquisition of 57 exclusive genes from, including genes important for virulence. A clade of three US localities, distant from one another, is under even faster evolutionary rates supported by core-coding, indels, and pangenome.
Fil: Patané, José S.L.. Universidade de Sao Paulo; Brasil
Fil: Martins, Joaquim. Universidade de Sao Paulo; Brasil
Fil: Castelão, Ana Beatriz. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Nishibe, Christiane. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Montera, Luciana. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Bigi, Fabiana. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Zumárraga, Martín José. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Cataldi, Ángel Adrián. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina
Fil: Junior, Antônio Fonseca. Ministerio da Agricultura Pecuaria e Abastecimento de Brasil. Empresa Brasileira de Pesquisa Agropecuaria; Brasil
Fil: Roxo, Eliana. Instituto Biológico de São Pablo; Brasil
Fil: Osório, Ana Luiza A. R.. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Jorge, Klaudia S.. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Thacker, Tyler C.. United States Department of Agriculture; Estados Unidos
Fil: Almeida, Nalvo F.. Universidade Federal do Mato Grosso do Sul; Brasil
Fil: Araújo, Flabio R.. Ministerio da Agricultura Pecuaria e Abastecimento de Brasil. Empresa Brasileira de Pesquisa Agropecuaria; Brasil
Fil: Setubal, João C.. Universidade de Sao Paulo; Brasil. Biocomplexity Institute of Virginia Tech; Estados Unidos
description Mycobacterium bovis is an important animal pathogen worldwide, parasitizing wild and domesticated vertebrate live stocks as well as humans. We investigated evolutionary patterns and processes in 38 sequenced genomes of M. bovis from the Americas, Europe, Asia, and Africa. We found that US strains are evolving distinctly (though with low magnitude) from most South American lineages regarding core-coding size, GC-content, and codon usage bias, and we further employ agreement to this pattern as proxy for phylogenetic reliability. Three data types were used for tree inference: 1. Single copy core-coding genes (core-coding); 2. Indel blocks coded as numeric characters (indels); 3. Gene presence/absence similarly coded (pangenome). Core-coding´s performance was below expected regarded we used 2,000+ genes, but indels and pangenome individually estimated reasonable trees, with HGT rates as high as 200x the DNA substitution rate. In addressing why core-coding performed poorly, we excluded phylogenetic method bias, homologous recombination, positive, and purifying selection as possible causes, whilst transient retention of random mildly deleterious mutations due to recent diversification, and also ongoing pseudogeneization, may be plausible. Although total evidence´s retention index was as good as presence/absence data individually in identifying US samples, it additionaly found a South American clade with more lineages excluding only two Brazilian samples. We further inferred divergence times using indels + pangenome due to lack of informativeness of core-coding, recovering relatively similar date estimates to previous studies on the origin of M. bovis (< 10,000 y) regardless of the dating prior (strict vs. uncorrelated clock, uniform vs. exponential clock, different age/rate standard deviation priors), evincing the suitability and unsuspected robustness of using strictly genomic-wide presence/absence data to dating, while also decisively rejecting a strict clock for our dataset. All trees supported a relatively basal position of African strains, which were isolated from Homo sapiens, suggesting it was an important region for early diversification and confirming we were one of the earliest hosts of the species. Evolution of US strains was affected by lateral acquisition of 57 exclusive genes from, including genes important for virulence. A clade of three US localities, distant from one another, is under even faster evolutionary rates supported by core-coding, indels, and pangenome.
publishDate 2017
dc.date.none.fl_str_mv 2017-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/72516
Patané, José S.L.; Martins, Joaquim; Castelão, Ana Beatriz; Nishibe, Christiane; Montera, Luciana; et al.; Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses; Oxford University Press; Genome Biology and Evolution; 9; 3; 3-2017; 521-535
1759-6653
CONICET Digital
CONICET
url http://hdl.handle.net/11336/72516
identifier_str_mv Patané, José S.L.; Martins, Joaquim; Castelão, Ana Beatriz; Nishibe, Christiane; Montera, Luciana; et al.; Patterns and Processes of Mycobacterium bovis Evolution Revealed by Phylogenomic Analyses; Oxford University Press; Genome Biology and Evolution; 9; 3; 3-2017; 521-535
1759-6653
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/doi/10.1093/gbe/evx022
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dc.publisher.none.fl_str_mv Oxford University Press
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