The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition

ABSTRACT Streptococcus pneumoniae is an important human pathogen that normally resides in the human nasopharynx. Competence-mediated bacteriocin expression by S. pneumoniae plays a major role in both the establishment and persistence of colonization on this polymicrobial surface. Over 20 distinct ba...

Full description

Saved in:
Bibliographic Details
Main Authors: J. D. Richardson, Emily Guo, Ryan M. Wyllie, Paul Jensen, Suzanne Dawid
Format: Article
Language:English
Published: American Society for Microbiology 2025-02-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.02993-24
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832096521370206208
author J. D. Richardson
Emily Guo
Ryan M. Wyllie
Paul Jensen
Suzanne Dawid
author_facet J. D. Richardson
Emily Guo
Ryan M. Wyllie
Paul Jensen
Suzanne Dawid
author_sort J. D. Richardson
collection DOAJ
description ABSTRACT Streptococcus pneumoniae is an important human pathogen that normally resides in the human nasopharynx. Competence-mediated bacteriocin expression by S. pneumoniae plays a major role in both the establishment and persistence of colonization on this polymicrobial surface. Over 20 distinct bacteriocin loci have been identified in pneumococcal genomes, but only a small number have been characterized phenotypically. In this work, we demonstrate that three-fourths of S. pneumoniae strains contain a highly conserved scb locus that encodes an active lactococcin 972-like bacteriocin called streptococcin B. In these backgrounds, the scbABC locus is part of the early competence cascade due to a ComE binding site in the promoter region. Streptococcin B producing strains target both members of the population that have failed to activate competence and the 25% of the population that carry a naturally occurring deletion of the ComE binding site and the functional bacteriocin gene. The ComR-type regulator found directly upstream of the scb locus in S. pneumoniae strains can activate scb expression independent of the presence of the ComE binding site but only when stimulated by a peptide that is encoded in the scb locus of Streptococcus pseudopneumoniae, a closely related bacterium that also inhabits the human nasopharynx. Given the co-regulation with competence and the phenotypic confirmation of activity, streptococcin B represents a previously unrecognized fratricide effector that gives producing strains an additional advantage over the naturally occurring deleted strains during colonization.IMPORTANCEStreptococcus pneumoniae is a common cause of pneumonia, meningitis, sinusitis, and otitis media. In order to successfully colonize humans, a prerequisite to the development of invasive disease, S. pneumoniae must compete with other bacterial inhabitants of the nasal surface for space and nutrients. Bacteriocins are small antimicrobial peptides produced by bacteria that typically target neighboring bacteria by disruption of the cell surface. S. pnuemoniae encodes a large number of potential bacteriocin, but, for most, their role in competitive interactions has not been defined. This work demonstrates that isolates that produce the bacteriocin streptococcin B have an advantage over non-producers. These observations contribute to our understanding of the competitive interactions that precede the development of S. pneumoniae disease.
format Article
id doaj-art-78d865af84024cb5b3d6e47c7345f2cf
institution Kabale University
issn 2150-7511
language English
publishDate 2025-02-01
publisher American Society for Microbiology
record_format Article
series mBio
spelling doaj-art-78d865af84024cb5b3d6e47c7345f2cf2025-02-05T14:00:48ZengAmerican Society for MicrobiologymBio2150-75112025-02-0116210.1128/mbio.02993-24The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competitionJ. D. Richardson0Emily Guo1Ryan M. Wyllie2Paul Jensen3Suzanne Dawid4Department of Pediatrics, University of Michigan, Ann Arbor, Michigan, USADepartment of Pediatrics, University of Michigan, Ann Arbor, Michigan, USADepartment of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USADepartment of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USADepartment of Pediatrics, University of Michigan, Ann Arbor, Michigan, USAABSTRACT Streptococcus pneumoniae is an important human pathogen that normally resides in the human nasopharynx. Competence-mediated bacteriocin expression by S. pneumoniae plays a major role in both the establishment and persistence of colonization on this polymicrobial surface. Over 20 distinct bacteriocin loci have been identified in pneumococcal genomes, but only a small number have been characterized phenotypically. In this work, we demonstrate that three-fourths of S. pneumoniae strains contain a highly conserved scb locus that encodes an active lactococcin 972-like bacteriocin called streptococcin B. In these backgrounds, the scbABC locus is part of the early competence cascade due to a ComE binding site in the promoter region. Streptococcin B producing strains target both members of the population that have failed to activate competence and the 25% of the population that carry a naturally occurring deletion of the ComE binding site and the functional bacteriocin gene. The ComR-type regulator found directly upstream of the scb locus in S. pneumoniae strains can activate scb expression independent of the presence of the ComE binding site but only when stimulated by a peptide that is encoded in the scb locus of Streptococcus pseudopneumoniae, a closely related bacterium that also inhabits the human nasopharynx. Given the co-regulation with competence and the phenotypic confirmation of activity, streptococcin B represents a previously unrecognized fratricide effector that gives producing strains an additional advantage over the naturally occurring deleted strains during colonization.IMPORTANCEStreptococcus pneumoniae is a common cause of pneumonia, meningitis, sinusitis, and otitis media. In order to successfully colonize humans, a prerequisite to the development of invasive disease, S. pneumoniae must compete with other bacterial inhabitants of the nasal surface for space and nutrients. Bacteriocins are small antimicrobial peptides produced by bacteria that typically target neighboring bacteria by disruption of the cell surface. S. pnuemoniae encodes a large number of potential bacteriocin, but, for most, their role in competitive interactions has not been defined. This work demonstrates that isolates that produce the bacteriocin streptococcin B have an advantage over non-producers. These observations contribute to our understanding of the competitive interactions that precede the development of S. pneumoniae disease.https://journals.asm.org/doi/10.1128/mbio.02993-24quorum sensingbacteriocinsStreptococcus pneumoniaegenetic competenceinterbacterial competition
spellingShingle J. D. Richardson
Emily Guo
Ryan M. Wyllie
Paul Jensen
Suzanne Dawid
The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition
mBio
quorum sensing
bacteriocins
Streptococcus pneumoniae
genetic competence
interbacterial competition
title The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition
title_full The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition
title_fullStr The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition
title_full_unstemmed The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition
title_short The pneumococcal bacteriocin streptococcin B is produced as part of the early competence cascade and promotes intraspecies competition
title_sort pneumococcal bacteriocin streptococcin b is produced as part of the early competence cascade and promotes intraspecies competition
topic quorum sensing
bacteriocins
Streptococcus pneumoniae
genetic competence
interbacterial competition
url https://journals.asm.org/doi/10.1128/mbio.02993-24
work_keys_str_mv AT jdrichardson thepneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT emilyguo thepneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT ryanmwyllie thepneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT pauljensen thepneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT suzannedawid thepneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT jdrichardson pneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT emilyguo pneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT ryanmwyllie pneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT pauljensen pneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition
AT suzannedawid pneumococcalbacteriocinstreptococcinbisproducedaspartoftheearlycompetencecascadeandpromotesintraspeciescompetition