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

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.

Bacillus wiedmannii biovar thuringiensis: a specialized mosquitocidal pathogen with plasmids from diverse origins

“…Strain FCC41 must have shared the ecological niche with other members of the B. cereus group. Our results support the hypothesis of cooperative infection, which predicts that conjugative plasmids carrying social genes such as Cry toxins could be widely distributed across clades ( Méric et al. 2018 ).…”

“…(2008) discussed that the global evolution of the B. cereus group seems to be strongly determined by ecological adaptations, being the temperature tolerance an important mechanism by which strains of the different groups adapted to novel environments and by which these groups have diverged. Most recently, Méric et al. (2018) reinforce this hypothesis proposing that the strains of different clades which share an ecological niche had increased opportunities for plasmid transfer between them.…”

Proposal of a Taxonomic Nomenclature for the Bacillus cereus Group Which Reconciles Genomic Definitions of Bacterial Species with Clinical and Industrial Phenotypes

“…Phenotypic characteristics used for taxonomic assignment of B. cereus group species (e.g., motility and hemolysis) vary within and among species (1,2,17,18). Furthermore, genomic determinants responsible for some phenotypes are plasmid mediated, such as synthesis of anthrax toxin/capsular proteins (19)(20)(21)(22), bioinsecticidal crystal proteins (23)(24)(25), and emetic toxin (cereulide) synthetase proteins (26,27). These traits can be lost, gained, heterogeneous in their presence within a species, or present across multiple species (28)(29)(30)(31).…”

BtToxin_Digger: a comprehensive and high-throughput pipeline for mining toxin protein genes from Bacillus thuringiensis

“…It can handle several assembled genomes every time and provide useful comparative results between the precited toxin and with known ones. During the past 7 years, it was widely used by researchers worldwide (Méric et al, 2018;Prado et al, 2014;Ruan et al, 2015;Zheng et al, 2017). Here we re-designed the previous tool to provide a novel, high-throughput, and local software BtToxin_Digger which can be directly used to handle large-scale genomic and metagenomic data to predict all kinds of putative toxin genes.…”