Genome Biol Evol. 2016 Mar 15. pii: evw055. [Epub ahead of print]

Diverse ecological strategies are encoded by Streptococcus pneumoniae bacteriocin-like peptides.

Miller EL1, Abrudan MI1, Roberts IS2, Rozen DE3.

Author information

Abstract

The opportunistic pathogen Streptococcus pneumoniae is commonly carried asymptomatically in the human nasopharynx. Due to high rates of co-colonization with other pneumococcus strains, intraspecific competitive interactions partly determine the carriage duration of strains and thereby their potential to cause disease. These interactions may be mediated by bacteriocins, such as the type IIb bacteriocins encoded by the blp (bacteriocin-like peptide) locus. To understand blp diversity and evolution, we undertook a bioinformatic analysis of 4,418 pneumococcal genomes, including 168 newly sequenced genomes. We describe immense variation at all levels of genomic organization: gene presence/absence, gene order, and allelic diversity. If we make the extreme and naive hypothesis that assumes all genes in this operon can assort randomly, this variation could lead to 1015 distinct bacteriocin-related phenotypes, each potentially representing a unique ecological strategy; however, we provide several explanations for why this extreme is not realized. Although rarefaction analysis indicates that the number of unique strategies is not saturated, even after sampling thousands of genomes, we show that the variation is neither unbounded nor random. We delimit three bacteriocin groups, which contain group-specific bacteriocins, immunity genes, and blp operon gene order, and argue that this organization places a constraint on realized ecological strategies. We additionally show that ecological strategy diversity is significantly constrained by pneumococcal phylogeny and clonal structure. By examining patterns of association between alleles within the blp operon, we show that bacteriocin genes, which were believed to function in pairs, can be found with a broad diversity of partner alleles and immunity genes; this overall lack of allelic fidelity likely contributes to the fluid structure of this operon. Our results clarify the diversity of antagonistic ecological strategies in the global pneumococcal population and highlight the potential role of blp bacteriocins in competition within the nasopharynx.

© The Author(s) 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

KEYWORDS:

antagonism; bacteriocin; bioinformatics; ecological strategies; interference competition

PMID: 26983823 [PubMed - as supplied by publisher]