Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Salmonella and Escherichia coli mannose-binding type 1 fimbriae exhibit highly similar receptor specificities, morphologies, and mechanisms of assembly but are nonorthologous in nature, i.e., not closely related evolutionarily. Their operons differ in chromosomal location, gene arrangement,...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Dagmara I. Kisiela, Sujay Chattopadhyay, Veronika Tchesnokova, Sandip Paul, Scott J. Weissman, Irena Medenica, Steven Clegg, Evgeni V. Sokurenko
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d397edb2657547a9a666f4dd00e882a6
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:d397edb2657547a9a666f4dd00e882a6
record_format	dspace
spelling	oai:doaj.org-article:d397edb2657547a9a666f4dd00e882a62021-11-15T15:40:27ZEvolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.00625-122150-7511https://doaj.org/article/d397edb2657547a9a666f4dd00e882a62013-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00625-12https://doaj.org/toc/2150-7511ABSTRACT Salmonella and Escherichia coli mannose-binding type 1 fimbriae exhibit highly similar receptor specificities, morphologies, and mechanisms of assembly but are nonorthologous in nature, i.e., not closely related evolutionarily. Their operons differ in chromosomal location, gene arrangement, and regulatory components. In the current study, we performed a comparative genetic and structural analysis of the major structural subunit, FimA, from Salmonella and E. coli and found that FimA pilins undergo diverse evolutionary adaptation in the different species. Whereas the E. coli fimA locus is characterized by high allelic diversity, frequent intragenic recombination, and horizontal movement, Salmonella fimA shows structural diversity that is more than 5-fold lower without strong evidence of gene shuffling or homologous recombination. In contrast to Salmonella FimA, the amino acid substitutions in the E. coli pilin heavily target the protein regions that are predicted to be exposed on the external surface of fimbriae. Altogether, our results suggest that E. coli, but not Salmonella, type 1 fimbriae display a high level of structural diversity consistent with a strong selection for antigenic variation under immune pressure. Thus, type 1 fimbriae in these closely related bacterial species appear to function in distinctly different physiological environments. IMPORTANCE E. coli and Salmonella are enteric bacteria that are closely related from an evolutionary perspective. They are both notorious human pathogens, though with somewhat distinct ecologies and virulence mechanisms. Type 1 fimbriae are rod-shaped surface appendages found in most E. coli and Salmonella isolates. In both species, they mediate bacterial adhesion to mannose receptors on host cells and share essentially the same morphology and assembly mechanisms. Here we show that despite the strong resemblances in function and structure, they are exposed to very different natural selection environments. Sequence analysis indicates that E. coli, but not Salmonella, fimbriae are subjected to strong immune pressure, resulting in a high level of major fimbrial protein gene shuffling and interbacterial transfer. Thus, evolutionary analysis tools can provide evidence of divergent physiological roles of functionally similar traits in different bacterial species.Dagmara I. KisielaSujay ChattopadhyayVeronika TchesnokovaSandip PaulScott J. WeissmanIrena MedenicaSteven CleggEvgeni V. SokurenkoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 2 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Dagmara I. Kisiela Sujay Chattopadhyay Veronika Tchesnokova Sandip Paul Scott J. Weissman Irena Medenica Steven Clegg Evgeni V. Sokurenko Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Salmonella and Escherichia coli mannose-binding type 1 fimbriae exhibit highly similar receptor specificities, morphologies, and mechanisms of assembly but are nonorthologous in nature, i.e., not closely related evolutionarily. Their operons differ in chromosomal location, gene arrangement, and regulatory components. In the current study, we performed a comparative genetic and structural analysis of the major structural subunit, FimA, from Salmonella and E. coli and found that FimA pilins undergo diverse evolutionary adaptation in the different species. Whereas the E. coli fimA locus is characterized by high allelic diversity, frequent intragenic recombination, and horizontal movement, Salmonella fimA shows structural diversity that is more than 5-fold lower without strong evidence of gene shuffling or homologous recombination. In contrast to Salmonella FimA, the amino acid substitutions in the E. coli pilin heavily target the protein regions that are predicted to be exposed on the external surface of fimbriae. Altogether, our results suggest that E. coli, but not Salmonella, type 1 fimbriae display a high level of structural diversity consistent with a strong selection for antigenic variation under immune pressure. Thus, type 1 fimbriae in these closely related bacterial species appear to function in distinctly different physiological environments. IMPORTANCE E. coli and Salmonella are enteric bacteria that are closely related from an evolutionary perspective. They are both notorious human pathogens, though with somewhat distinct ecologies and virulence mechanisms. Type 1 fimbriae are rod-shaped surface appendages found in most E. coli and Salmonella isolates. In both species, they mediate bacterial adhesion to mannose receptors on host cells and share essentially the same morphology and assembly mechanisms. Here we show that despite the strong resemblances in function and structure, they are exposed to very different natural selection environments. Sequence analysis indicates that E. coli, but not Salmonella, fimbriae are subjected to strong immune pressure, resulting in a high level of major fimbrial protein gene shuffling and interbacterial transfer. Thus, evolutionary analysis tools can provide evidence of divergent physiological roles of functionally similar traits in different bacterial species.
format	article
author	Dagmara I. Kisiela Sujay Chattopadhyay Veronika Tchesnokova Sandip Paul Scott J. Weissman Irena Medenica Steven Clegg Evgeni V. Sokurenko
author_facet	Dagmara I. Kisiela Sujay Chattopadhyay Veronika Tchesnokova Sandip Paul Scott J. Weissman Irena Medenica Steven Clegg Evgeni V. Sokurenko
author_sort	Dagmara I. Kisiela
title	Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	evolutionary analysis points to divergent physiological roles of type 1 fimbriae in <italic toggle="yes">salmonella</italic> and <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/d397edb2657547a9a666f4dd00e882a6
work_keys_str_mv	AT dagmaraikisiela evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT sujaychattopadhyay evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT veronikatchesnokova evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT sandippaul evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT scottjweissman evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT irenamedenica evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT stevenclegg evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT evgenivsokurenko evolutionaryanalysispointstodivergentphysiologicalrolesoftype1fimbriaeinitalictoggleyessalmonellaitalicandnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent
_version_	1718427732271955968

Evolutionary Analysis Points to Divergent Physiological Roles of Type 1 Fimbriae in <italic toggle="yes">Salmonella</italic> and <named-content content-type="genus-species">Escherichia coli</named-content>

Ejemplares similares