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While these organisms often resist\n              <jats:italic toggle=\"yes\">in vitro<\/jats:italic>\n              culture, they multiply both in plant sieve elements and hemipteran vectors. Such cross-kingdom parasitic lifestyle has emerged in diverse taxa via distinct ecological routes. In the genus\n              <jats:italic toggle=\"yes\">Arsenophonus<\/jats:italic>\n              , the phloem pathogens \u201c\n              <jats:italic toggle=\"yes\">Candidatus<\/jats:italic>\n              Arsenophonus phytopathogenicus\u201d (Ap) and \u201c\n              <jats:italic toggle=\"yes\">Ca<\/jats:italic>\n              . Phlomobacter fragariae\u201d (Pf) have evolved from insect endosymbionts, but the genetic mechanisms underlying this transition have not been explored. To fill this gap, we obtained the genomes of both strains from insect host metagenomes. The resulting assemblies are highly similar in size and functional repertoire, rich in viral sequences, and closely resemble the genomes of several facultative endosymbiotic\n              <jats:italic toggle=\"yes\">Arsenophonus<\/jats:italic>\n              strains of sap-sucking hemipterans. However, a phylogenomic analysis demonstrated distinct origins, as Ap belongs to the \u201c\n              <jats:italic toggle=\"yes\">Triatominarum<\/jats:italic>\n              \u201d clade, whereas Pf represents a distant species. We identified a set of orthologs encoded only by Ap and Pf in the genus, including hydrolytic enzymes likely targeting plant substrates. In particular, both bacteria encode putative plant cell wall-degrading enzymes and cysteine peptidases related to xylellain, a papain-like peptidase from\n              <jats:italic toggle=\"yes\">Xylella fastidiosa<\/jats:italic>\n              , for which close homologs are found in diverse\n              <jats:italic toggle=\"yes\">Pseudomonadota<\/jats:italic>\n              infecting the plant vasculature.\n              <jats:italic toggle=\"yes\">In silico<\/jats:italic>\n              predictions and gene expression analyses further support a role during phloem colonization for several of the shared orthologs. We conclude that the double emergence of phytopathogenicity in\n              <jats:italic toggle=\"yes\">Arsenophonus<\/jats:italic>\n              may have been mediated by a few horizontal gene transfer events, involving genes acquired from other\n              <jats:italic toggle=\"yes\">Pseudomonadota<\/jats:italic>\n              , including phytopathogens.\n            <\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>IMPORTANCE<\/jats:title>\n            <jats:p>\n              We investigate the genetic mechanisms of a transition in bacterial lifestyle. We focus on two phloem pathogens belonging to the genus\n              <jats:italic toggle=\"yes\">Arsenophonus<\/jats:italic>\n              : \u201c\n              <jats:italic toggle=\"yes\">Candidatus<\/jats:italic>\n              Arsenophonus phytopathogenicus\u201d and \u201c\n              <jats:italic toggle=\"yes\">Ca<\/jats:italic>\n              . Phlomobacter fragariae.\u201d 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\n              <jats:italic toggle=\"yes\">Arsenophonus<\/jats:italic>\n              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\n              <jats:italic toggle=\"yes\">Arsenophonus<\/jats:italic>\n              strains.\n            <\/jats:p>\n          <\/jats:sec>","DOI":"10.1128\/msystems.01496-24","type":"journal-article","created":{"date-parts":[[2025,4,9]],"date-time":"2025-04-09T13:00:48Z","timestamp":1744203648000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":11,"title":["From insect endosymbiont to phloem colonizer: comparative genomics unveils the lifestyle transition of phytopathogenic\n            <i>Arsenophonus<\/i>\n            strains"],"prefix":"10.1128","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1974-7863","authenticated-orcid":true,"given":"Mathieu","family":"Mahillon","sequence":"first","affiliation":[{"name":"Research group Virology, Bacteriology and 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LM Konstantinidis KT. 2016. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. 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