Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters

ABSTRACT All fully sequenced strains of Streptococcus pneumoniae possess a version of the blp locus, which is responsible for bacteriocin production and immunity. Activation of the blp locus is stimulated by accumulation of the peptide pheromone, BlpC, following its secretion by the ABC transporter,...

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Autores principales:	Matthew R. Son, Mikhail Shchepetov, Peter V. Adrian, Shabir A. Madhi, Linda de Gouveia, Anne von Gottberg, Keith P. Klugman, Jeffrey N. Weiser, Suzanne Dawid
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c4c6d6e1d5b84d9293621799c5df903a
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spelling	oai:doaj.org-article:c4c6d6e1d5b84d9293621799c5df903a2021-11-15T15:38:58ZConserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters10.1128/mBio.00179-112150-7511https://doaj.org/article/c4c6d6e1d5b84d9293621799c5df903a2011-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00179-11https://doaj.org/toc/2150-7511ABSTRACT All fully sequenced strains of Streptococcus pneumoniae possess a version of the blp locus, which is responsible for bacteriocin production and immunity. Activation of the blp locus is stimulated by accumulation of the peptide pheromone, BlpC, following its secretion by the ABC transporter, BlpA. The blp locus is characterized by significant diversity in blpC type and in the region of the locus containing putative bacteriocin and immunity genes. In addition, the blpA gene can represent a single large open reading frame or be divided into several smaller fragments due to the presence of frameshift mutations. In this study, we use a collection of strains with blp-dependent inhibition and immunity to define the genetic changes that bring about phenotypic differences in bacteriocin production or immunity. We demonstrate that alterations in blpA, blpC, and bacteriocin/immunity content likely play an important role in competitive interactions between pneumococcal strains. Importantly, strains with a highly conserved frameshift mutation in blpA are unable to secrete bacteriocins or BlpC, but retain the ability to respond to exogenous peptide pheromone produced by cocolonizing strains, stimulating blp-mediated immunity. These “cheater” strains can only coexist with bacteriocin-producing strains that secrete their cognate BlpC and share the same immunity proteins. The variable outcome of these interactions helps to explain the heterogeneity of the blp pheromone, bacteriocin, and immunity protein content. IMPORTANCE Streptococcus pneumoniae resides in a polymicrobial environment and competes for limited resources by the elaboration of small antimicrobial peptides called bacteriocins. A conserved cluster of genes in the S. pneumoniae genome is involved in the production of bacteriocins and their associated protective immunity proteins through secretion of a signaling pheromone. In this study, we show that a significant number of strains have lost the ability to secrete bacteriocins and signaling pheromones due to a specific mutation in a dedicated transporter protein. Because the regulatory and immunity portion of the locus is retained, these “cheater” strains can survive in the face of invasion from a bacteriocin-producing strain without the cost of bacteriocin secretion. The outcome of such interactions depends on each strain’s repertoire of pheromone, immunity protein, and bacteriocin genes, such that intrastrain competition drives the diversity in bacteriocin, immunity protein, and pheromone content.Matthew R. SonMikhail ShchepetovPeter V. AdrianShabir A. MadhiLinda de GouveiaAnne von GottbergKeith P. KlugmanJeffrey N. WeiserSuzanne DawidAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 5 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Matthew R. Son Mikhail Shchepetov Peter V. Adrian Shabir A. Madhi Linda de Gouveia Anne von Gottberg Keith P. Klugman Jeffrey N. Weiser Suzanne Dawid Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters
description	ABSTRACT All fully sequenced strains of Streptococcus pneumoniae possess a version of the blp locus, which is responsible for bacteriocin production and immunity. Activation of the blp locus is stimulated by accumulation of the peptide pheromone, BlpC, following its secretion by the ABC transporter, BlpA. The blp locus is characterized by significant diversity in blpC type and in the region of the locus containing putative bacteriocin and immunity genes. In addition, the blpA gene can represent a single large open reading frame or be divided into several smaller fragments due to the presence of frameshift mutations. In this study, we use a collection of strains with blp-dependent inhibition and immunity to define the genetic changes that bring about phenotypic differences in bacteriocin production or immunity. We demonstrate that alterations in blpA, blpC, and bacteriocin/immunity content likely play an important role in competitive interactions between pneumococcal strains. Importantly, strains with a highly conserved frameshift mutation in blpA are unable to secrete bacteriocins or BlpC, but retain the ability to respond to exogenous peptide pheromone produced by cocolonizing strains, stimulating blp-mediated immunity. These “cheater” strains can only coexist with bacteriocin-producing strains that secrete their cognate BlpC and share the same immunity proteins. The variable outcome of these interactions helps to explain the heterogeneity of the blp pheromone, bacteriocin, and immunity protein content. IMPORTANCE Streptococcus pneumoniae resides in a polymicrobial environment and competes for limited resources by the elaboration of small antimicrobial peptides called bacteriocins. A conserved cluster of genes in the S. pneumoniae genome is involved in the production of bacteriocins and their associated protective immunity proteins through secretion of a signaling pheromone. In this study, we show that a significant number of strains have lost the ability to secrete bacteriocins and signaling pheromones due to a specific mutation in a dedicated transporter protein. Because the regulatory and immunity portion of the locus is retained, these “cheater” strains can survive in the face of invasion from a bacteriocin-producing strain without the cost of bacteriocin secretion. The outcome of such interactions depends on each strain’s repertoire of pheromone, immunity protein, and bacteriocin genes, such that intrastrain competition drives the diversity in bacteriocin, immunity protein, and pheromone content.
format	article
author	Matthew R. Son Mikhail Shchepetov Peter V. Adrian Shabir A. Madhi Linda de Gouveia Anne von Gottberg Keith P. Klugman Jeffrey N. Weiser Suzanne Dawid
author_facet	Matthew R. Son Mikhail Shchepetov Peter V. Adrian Shabir A. Madhi Linda de Gouveia Anne von Gottberg Keith P. Klugman Jeffrey N. Weiser Suzanne Dawid
author_sort	Matthew R. Son
title	Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters
title_short	Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters
title_full	Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters
title_fullStr	Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters
title_full_unstemmed	Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters
title_sort	conserved mutations in the pneumococcal bacteriocin transporter gene, <italic toggle="yes">blpa</italic>, result in a complex population consisting of producers and cheaters
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/c4c6d6e1d5b84d9293621799c5df903a
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Conserved Mutations in the Pneumococcal Bacteriocin Transporter Gene, <italic toggle="yes">blpA</italic>, Result in a Complex Population Consisting of Producers and Cheaters

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