Impact of homologous recombination on core genome evolution and host adaptation ofPectobacterium parmentieri

Abstract

AbstractHomologous recombination is a major force mechanism driving bacterial evolution, host adaptability and acquisition of novel virulence traits.Pectobacterium parmentieriis a plant bacterial pathogen distributed worldwide, primarily affecting potatoes, by causing soft rot and blackleg diseases. The goal of this investigation was to understand the impact of homologous recombination on the genomic evolution ofP. parmentieri. Analysis ofP. parmentierigenomes using Roary revealed a dynamic pan-genome with 3,742 core genes and over 55% accessory genome variability. Bayesian population structure analysis identified seven lineages, indicating species heterogeneity. ClonalFrameML analysis displayed 5,125 recombination events, with the lineage 4 exhibiting the highest events. FastGEAR analysis identified 486 ancestral and 941 recent recombination events ranging 43 bp - 119 kb and 36 bp - 13.96 kb, respectively, suggesting ongoing adaptation. Notably, 11% (412 genes) of the core genome underwent recent recombination, with lineage 1 as the main donor. The prevalence of recent recombination (double compared to ancient) events implies continuous adaptation, possibly driven by global potato trade. Recombination events were found in vital cellular processes (DNA replication, DNA repair, RNA processing, homeostasis, and metabolism), pathogenicity determinants (type secretion systems, cell-wall degrading enzymes, iron scavengers, lipopolysaccharides, flagellum, etc.), antimicrobial compounds (phenazine and colicin) and even CRISPR-Cas genes. Overall, these results emphasize the role of homologous recombination inP. parmentieri’s evolutionary dynamics, influencing host colonization, pathogenicity, adaptive immunity, and ecological fitness.SignificanceThis study explores the influence of homologous recombination on the genomic evolution of the globally distributed plant pathogenP. parmentieri, characterized by highly heterogenous strains from various global locations. Our findings reveal diverse recombinogenic patterns within the core genomes ofP. parmentieriisolates, notably in genomic loci associated with vital cell functions, pathogenicity determinants, and CRISPR-Cas genes. These findings highlight the role of homologous recombination in shaping the genomes ofP. parmentieriand impacting its phytopathogenic lifestyle. Additionally, the data suggest a potential role of recombination in the ecological adaptation of this species across different climates, providing insights into the worldwide presence ofP. parmentieri. This study represents a pioneering exploration of the impact of homologous recombination on the dynamic evolutionary genomics of the soft rot-causing bacteriumP. parmentieri.