Abstract
Bacterial plasmids can vary from small selfish genetic elements to large autonomous replicons that constitute a significant proportion of total cellular DNA. By conferring novel function to the cell, plasmids may facilitate evolution but their mobility may be opposed by co‐evolutionary relationships with chromosomes or encouraged via the infectious sharing of genes encoding public goods. Here, we explore these hypotheses through large‐scale examination of the association between plasmids and chromosomal DNA 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 characterized population genomic structure, gene content and plasmid distribution to investigate 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 and genes from 410 reference 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 variable gene content, a pattern of plasmid segregation consistent with transfer during infectious cooperation. Nevertheless, comparison between clades suggests that co‐evolutionary interactions may drive association between 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.
Highlights
A recurring feature of the genome organization of many pathogenic bacteria is that important virulence factors are often encoded on horizontally mobile genetic elements (MGEs) (Hacker and Carniel 2001, Sansonetti et al 1981, Smith 2001)
Isolate genomes within the B. cereus group show evidence of horizontal gene transfer (HGT), consistent with previous work (Van der Auwera et al 2007, Vilas-Bôas et al 2008) (Didelot et al 2009)
B. cereus group containing B. thuringiensis (Bt), B. cereus sensu stricto (Bc), B. anthracis (Ba), B. mycoides, B. weihenstephanensis should be treated as one species (Helgason et al 2000, Tourasse et al 2006)
Summary
A recurring feature of the genome organization of many pathogenic bacteria is that important virulence factors are often encoded on horizontally mobile genetic elements (MGEs) (Hacker and Carniel 2001, Sansonetti et al 1981, Smith 2001). Many pathogenic bacteria carry essential virulence genes on plasmids, sometimes even when there is ecological and genomic evidence indicating that they are obligate pathogens or compete and replicate poorly in the environment (Hugh-Jones and Blackburn 2009, Keim et al 2009, Yang 2005, Yara et al1997). There are several competing, not necessarily mutually exclusive hypotheses, that explain why some genes are carried on mobile elements and why bacterial virulence factors, in particular, tend to be mobile. This includes the theory that hot spots for recombination occur on the accessory genome. Genes may be able to persist in plasmids through hitch-hiking with beneficial genes or alleles ensuring that plasmids are maintained by periodically rising to high frequencies via selection on these traits (Bergstrom et al 2000)
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