Rapid dissemination of host-metabolism-manipulating transposon-like entities via integrative and conjugative elements

Abstract

Integrative and conjugative elements (ICEs) are self-transmissible mobile elements that transfer functional genetic units across broad phylogenetic distances. Accessory genes shuttled by ICEs can make significant contributions to bacterial fitness, yet ICEs that carry accessory genes encoding functions other than antimicrobial resistance remain poorly characterized. Recent observation of the rapid acquisition of ICEs in a pandemic lineage of Pseudomonas syringae pv. actinidae led to investigation of the structural and functional diversity of these elements among a diverse array of P. syringae. Fifty-three unique ICE types were identified across multiple phylogroups. These ICEs display distinct evolutionary histories compared to their bacterial hosts, are highly recombinogenic, exhibit a conserved structure and are punctuated by hotspots of accessory gene integration. Many carry a 16 kb transposon-like entity (Tn6212) that shows little polymorphism indicating recent dissemination. Deletion of Tn6212 did not alter pathogen growth in planta, but mutants displayed significant fitness defects when grown on TCA cycle intermediates. These were largely attributable to a single LysR regulator. RNA-seq analysis of a set of nested Tn6212 deletions confirmed a central role of LysR in enhanced expression of more than 300 genes and down-regulation of genes controlling expression of energetically demanding loci. Together the transcriptional data indicate a major role for Tn6212 in manipulation of bacterial metabolism with primary effects on RNA degradation, protein synthesis and potential diversion of ATP to growth.