From insect endosymbiont to phloem colonizer: comparative genomics unveils the lifestyle transition of phytopathogenic <i>Arsenophonus</i> strains

We investigate the genetic mechanisms of a transition in bacterial lifestyle. We focus on two phloem pathogens belonging to the genus <i>Arsenophonus</i>: "<i>Candidatus</i> Arsenophonus phytopathogenicus" and "<i>Ca</i>. Phlomobacter fragariae." Both bacteria cause economically significant pathologies, and they have likely emerged among facultative insect endosymbionts. Our genomic analyses show that both strains are highly similar to other strains of the genus associated with sap-sucking hemipterans, suggesting a recent lifestyle shift. Importantly, although the phytopathogenic <i>Arsenophonus</i> strains belong to distant clades, they share a small set of orthologs unique in the genus pangenome. We provide evidence that several of these genes produce hydrolytic enzymes that are secreted and may target plant substrates. The acquisition and exchange of these genes may thus have played a pivotal role in the lifestyle transition of the phytopathogenic <i>Arsenophonus</i> strains.