Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group

Abstract

Bacterial plasmids have roles that range from large secondary chromosomes to small selfish genetic elements. Distinct, but not necessarily mutually exclusive theories have been proposed to resolve plasmid bacteria relationships: plasmids may facilitate evolutionary novelty and maintain beneficial genes via hitchhiking, while plasmid mobility may be opposed by coevolutionary relationships with chromosomes or encouraged via the infectious sharing of genes encoding public goods. Here, we sought to explore a range of these hypotheses through a large-scale examination of the association between plasmids and genomes in the phenotypically diverse Bacillus cereus group. This complex group is rich in plasmids, many of which encode essential virulence factors (Cry toxins) that are known public goods. We aimed to characterize population genomic structure, examine the dynamics of plasmid distribution and gene content and the role of mobile elements in diversification.. We analysed coding sequence within the core and accessory genome of 190 B. cereus group isolates, including 23 novel sequences, including plasmid genes from a reference collection of 410 plasmid genomes. While cry genes were widely distributed, those with invertebrate toxicity were predominantly associated with one sequence cluster (clade 2) and phenotypically defined Bacillus thuringiensis. Cry toxin plasmids in clade 2 showed evidence of recent horizontal transfer and dynamic gene content, a pattern of plasmid segregation consistent with transfer during infectious cooperation. Nevertheless, comparison between clades suggests that coevolutionary interactions may drive association of plasmids and chromosomes and limit wider transfer of key virulence traits. Proliferation of successful plasmid and chromosome combinations is a feature of specialized pathogens with characteristic niches (Bacillus anthracis, B. thuringiensis) and has occurred multiple times in the B. cereus group