Bacterial Evolution by Genomic Island Transfer Occurs via DNA Transformation In Planta

Abstract

Our understanding of the evolution of microbial pathogens has been advanced by the discovery of "islands" of DNA that differ from core genomes and contain determinants of virulence. The acquisition of genomic islands (GIs) by horizontal gene transfer (HGT) is thought to have played a major role in microbial evolution. There are, however, few practical demonstrations of the acquisition of genes that control virulence, and, significantly, all have been achieved outside the animal or plant host. Loss of a GI from the bean pathogen Pseudomonas syringae pv. phaseolicola (Pph) is driven by exposure to the stress imposed by the plant's resistance response. Here, we show that the complete episomal island, which carries pathogenicity genes including the effector avrPphB, transfers between strains of Pph by transformation in planta and inserts at a specific att site in the genome of the recipient. Our results show that the evolution of bacterial pathogens by HGT may be achieved via transformation, the simplest mechanism of DNA exchange. This process is activated by exposure to plant defenses, when the pathogen is in greatest need of acquiring new genetic traits to alleviate the antimicrobial stress imposed by plant innate immunity.

Host immune responses accelerate pathogen evolution

“…Similar results have been reported previously where an experimental evolution approach was used to investigate pathogen adaptation in completely unrelated environments such as mouse macrophage (Ensminger et al, 2012) and cystic fibrosis-like culture conditions in the presence and absence of fluoroquinolone antibiotics . In addition, unlike some other studies of the pathogen evolution in planta (Pitman et al, 2005;Lovell et al, 2009), our analysis did not detect the complete loss or gain of any gene among the bacterial strains compared with the parent.…”

The influence of the accessory genome on bacterial pathogen evolution

“…87 Moreover, it raises the question of whether other recombinases (e.g., those of ICEs, GIs, IS elements and transposons) are also affected by conjugation and regulated by LexA and the SOS response-certainly, stress affects P. syringae PPHGI-1 integrase expression. [58][59][60]88,89 Integrons have been found in a wide range of non-pathogenic and pathogenic bacteria in environments ranging from marine to terrestrial organisms and niches. 73,77,83,[90][91][92][93][94][95][96][97][98][99][100][101] Two types of integrons, the chromosomal integron (CI) and mobile integron (MI) have been identified: 70 CIs appear to represent a "core" gene capture system in Gram negative bacteria to enable genome flexibility for adaptation to diverse environments.…”

“…78 Clearly, the host environment as well as the antibiotic treatment are likely to be influencing integron transfer on MGEs, a similar situation as seen with ICEs. 60 An interesting observation by van der Veen et al 102 was that the prevalence of integrons within the intestinal microbial populations decreased despite continued antibiotic treatment. This may indicate that there is a cost to the bacteria of carrying either the integron or its shuttle element.…”

“…59 In fact it has been demonstrated that PPHGI-1 is mobile and can be acquired by another Pph strain via transformation in planta. 60 Bioinformatic analysis of whole genome sequences has revealed that a number of GIs are predicted to occur in any given strain and deciphering which ones are involved in virulence is a laborious task. 61,62 Lloyd et al 61 investigated this by individually deleting 11 of the predicted 13 GIs in the uropathogenic E. coli strain CFT073.…”

Hydrogen sulfide causes excision of a genomic island in Pseudomonas syringae pv. phaseolicola

“…Pitman et al (2005) further demonstrated that the integrase gene xerC (PPHGI-1 ORF.100) is required for GI excision and that xerC transcriptional expression is greatly increased (50 times) in leaves undergoing the HR compared to in vitro conditions. Furthermore, Lovell et al (2009Lovell et al ( , 2011 demonstrated that PPHGI-1 can be transferred between strains of Pph via natural transformation and is able to integrate into the recipient strains chromosome.…”