Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species

ABSTRACT The distribution, genome location, and evolution of the four paralogous zinc metalloproteases, IgA1 protease, ZmpB, ZmpC, and ZmpD, in Streptococcus pneumoniae and related commensal species were studied by in silico analysis of whole genomes and by activity screening of 154 representatives...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Malene Bek-Thomsen, Knud Poulsen, Mogens Kilian
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ee0e09344dc041378108103d3b377ec2
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:ee0e09344dc041378108103d3b377ec2
record_format	dspace
spelling	oai:doaj.org-article:ee0e09344dc041378108103d3b377ec22021-11-15T15:39:12ZOccurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species10.1128/mBio.00303-122150-7511https://doaj.org/article/ee0e09344dc041378108103d3b377ec22012-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00303-12https://doaj.org/toc/2150-7511ABSTRACT The distribution, genome location, and evolution of the four paralogous zinc metalloproteases, IgA1 protease, ZmpB, ZmpC, and ZmpD, in Streptococcus pneumoniae and related commensal species were studied by in silico analysis of whole genomes and by activity screening of 154 representatives of 20 species. ZmpB was ubiquitous in the Mitis and Salivarius groups of the genus Streptococcus and in the genera Gemella and Granulicatella, with the exception of a fragmented gene in Streptococcus thermophilus, the only species with a nonhuman habitat. IgA1 protease activity was observed in all members of S. pneumoniae, S. pseudopneumoniae, S. oralis, S. sanguinis, and Gemella haemolysans, was variably present in S. mitis and S. infantis, and absent in S. gordonii, S. parasanguinis, S. cristatus, S. oligofermentans, S. australis, S. peroris, and S. suis. Phylogenetic analysis of 297 zmp sequences and representative housekeeping genes provided evidence for an unprecedented selection for genetic diversification of the iga, zmpB, and zmpD genes in S. pneumoniae and evidence of very frequent intraspecies transfer of entire genes and combination of genes. Presumably due to their adaptation to a commensal lifestyle, largely unaffected by adaptive mucosal immune factors, the corresponding genes in commensal streptococci have remained conserved. The widespread distribution and significant sequence diversity indicate an ancient origin of the zinc metalloproteases predating the emergence of the humanoid species. zmpB, which appears to be the ancestral gene, subsequently duplicated and successfully diversified into distinct functions, is likely to serve an important but yet unknown housekeeping function associated with the human host. IMPORTANCE The paralogous zinc metalloproteases IgA1 protease, ZmpB, ZmpC, and ZmpD have been identified as crucial for virulence of the human pathogen Streptococcus pneumoniae. This study maps the presence of the corresponding genes and enzyme activities in S. pneumoniae and in related commensal species of the genera Streptococcus, Gemella, and Granulicatella. The distribution, genome location, and sequence diversification indicate that zmpB is the ancestral gene predating the evolution of today’s humanoid species. The ZmpB protease may play an important but yet unidentified role in the association of streptococci of the Mitis and Salivarius groups with their human host, as it is ubiquitous in these two groups, except for a fragmented gene in Streptococcus thermophilus, the only species not associated with humans. The relative sequence diversification of the IgA1 protease, ZmpB, and ZmpD is striking evidence of differences in selection for diversification of these surface-exposed proteins in the pathogen S. pneumoniae compared to the closely related commensal streptococci.Malene Bek-ThomsenKnud PoulsenMogens KilianAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 5 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Malene Bek-Thomsen Knud Poulsen Mogens Kilian Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species
description	ABSTRACT The distribution, genome location, and evolution of the four paralogous zinc metalloproteases, IgA1 protease, ZmpB, ZmpC, and ZmpD, in Streptococcus pneumoniae and related commensal species were studied by in silico analysis of whole genomes and by activity screening of 154 representatives of 20 species. ZmpB was ubiquitous in the Mitis and Salivarius groups of the genus Streptococcus and in the genera Gemella and Granulicatella, with the exception of a fragmented gene in Streptococcus thermophilus, the only species with a nonhuman habitat. IgA1 protease activity was observed in all members of S. pneumoniae, S. pseudopneumoniae, S. oralis, S. sanguinis, and Gemella haemolysans, was variably present in S. mitis and S. infantis, and absent in S. gordonii, S. parasanguinis, S. cristatus, S. oligofermentans, S. australis, S. peroris, and S. suis. Phylogenetic analysis of 297 zmp sequences and representative housekeeping genes provided evidence for an unprecedented selection for genetic diversification of the iga, zmpB, and zmpD genes in S. pneumoniae and evidence of very frequent intraspecies transfer of entire genes and combination of genes. Presumably due to their adaptation to a commensal lifestyle, largely unaffected by adaptive mucosal immune factors, the corresponding genes in commensal streptococci have remained conserved. The widespread distribution and significant sequence diversity indicate an ancient origin of the zinc metalloproteases predating the emergence of the humanoid species. zmpB, which appears to be the ancestral gene, subsequently duplicated and successfully diversified into distinct functions, is likely to serve an important but yet unknown housekeeping function associated with the human host. IMPORTANCE The paralogous zinc metalloproteases IgA1 protease, ZmpB, ZmpC, and ZmpD have been identified as crucial for virulence of the human pathogen Streptococcus pneumoniae. This study maps the presence of the corresponding genes and enzyme activities in S. pneumoniae and in related commensal species of the genera Streptococcus, Gemella, and Granulicatella. The distribution, genome location, and sequence diversification indicate that zmpB is the ancestral gene predating the evolution of today’s humanoid species. The ZmpB protease may play an important but yet unidentified role in the association of streptococci of the Mitis and Salivarius groups with their human host, as it is ubiquitous in these two groups, except for a fragmented gene in Streptococcus thermophilus, the only species not associated with humans. The relative sequence diversification of the IgA1 protease, ZmpB, and ZmpD is striking evidence of differences in selection for diversification of these surface-exposed proteins in the pathogen S. pneumoniae compared to the closely related commensal streptococci.
format	article
author	Malene Bek-Thomsen Knud Poulsen Mogens Kilian
author_facet	Malene Bek-Thomsen Knud Poulsen Mogens Kilian
author_sort	Malene Bek-Thomsen
title	Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species
title_short	Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species
title_full	Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species
title_fullStr	Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species
title_full_unstemmed	Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species
title_sort	occurrence and evolution of the paralogous zinc metalloproteases iga1 protease, zmpb, zmpc, and zmpd in <named-content content-type="genus-species">streptococcus pneumoniae</named-content> and related commensal species
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/ee0e09344dc041378108103d3b377ec2
work_keys_str_mv	AT malenebekthomsen occurrenceandevolutionoftheparalogouszincmetalloproteasesiga1proteasezmpbzmpcandzmpdinnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentandrelatedcommensalspecies AT knudpoulsen occurrenceandevolutionoftheparalogouszincmetalloproteasesiga1proteasezmpbzmpcandzmpdinnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentandrelatedcommensalspecies AT mogenskilian occurrenceandevolutionoftheparalogouszincmetalloproteasesiga1proteasezmpbzmpcandzmpdinnamedcontentcontenttypegenusspeciesstreptococcuspneumoniaenamedcontentandrelatedcommensalspecies
_version_	1718427802063077376

Occurrence and Evolution of the Paralogous Zinc Metalloproteases IgA1 Protease, ZmpB, ZmpC, and ZmpD in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> and Related Commensal Species

Ejemplares similares