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The cosmopolitan cat (\n Ctenocephalides felis<\/jats:italic>\n ) and dog (\n Ctenocephalides canis<\/jats:italic>\n ) fleas, as well as\n Ctenocephalides orientis<\/jats:italic>\n (restricted to tropical and subtropical Asia), breed in human dwellings and are vectors of cat-scratch fever (caused by\n \n \n Bartonella<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n spp.) and\n \n \n Rickettsia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n spp., including\n \n \n Rickettsia felis<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n (agent of flea-borne spotted fever) and\n \n \n Rickettsia asembonensis<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n , a suspected pathogen. These\n \n \n Rickettsia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n spp. are members of a phylogenetic clade known as the \u2018transitional group\u2019, which includes both human pathogens and arthropod-specific endosymbionts. The relatively depauperate flea microbiome can also contain other endosymbionts, including a diverse range of\n \n \n Wolbachia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n strains. Here, we present circularized genome assemblies for two\n C. orientis<\/jats:italic>\n -derived pathogens (\n \n \n Bartonella clarridgeiae<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n and\n \n \n R. asembonensis<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n ) from Malaysia, a novel\n \n \n Wolbachia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n strain (\n w<\/jats:italic>\n Cori), and the\n C. orientis<\/jats:italic>\n mitochondrion; all were obtained by direct metagenomic sequencing of flea tissues. Moreover, we isolated two\n \n \n Wolbachia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n strains from Malaysian\n C. felis<\/jats:italic>\n into tick cell culture and recovered circularized genome assemblies for both, one of which (\n w<\/jats:italic>\n CfeF) is newly sequenced. We demonstrate that the three\n \n \n Wolbachia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n strains are representatives of different major clades (\u2018supergroups\u2019), two of which appear to be flea-specific. These\n \n \n Wolbachia<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n genomes exhibit unique combinations of features associated with reproductive parasitism or mutualism, including prophage WO, cytoplasmic incompatibility factors and the biotin operon of obligate intracellular microbes. The first circularized assembly for\n \n \n R. asembonensis<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n includes a plasmid with a markedly different structure and gene content compared to the published plasmid; moreover, this novel plasmid was also detected in cat flea metagenomes from the USA. Analysis of loci under positive selection in the transitional group revealed genes involved in host\u2013pathogen interactions that may facilitate host switching. Finally, the first\n \n \n B. clarridgeiae<\/jats:ext-link>\n <\/jats:named-content>\n <\/jats:italic>\n genome from Asia exhibited large-scale genome stability compared to isolates from other continents, except for SNPs in regions predicted to mediate interactions with the vertebrate host. These findings highlight the paucity of data on the genomic diversity of\n Ctenocephalides<\/jats:italic>\n -associated bacteria and raise questions regarding how interactions between members of the flea microbiome might influence vector competence.\n <\/jats:p>","DOI":"10.1099\/mgen.0.001045","type":"journal-article","created":{"date-parts":[[2023,7,3]],"date-time":"2023-07-03T12:16:14Z","timestamp":1688386574000},"source":"Crossref","is-referenced-by-count":16,"title":["Metagenomics of culture isolates and insect tissue illuminate the evolution of Wolbachia, Rickettsia and Bartonella symbionts in Ctenocephalides spp. fleas"],"prefix":"10.1099","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1194-5689","authenticated-orcid":false,"given":"Alexandra","family":"Beliavskaia","sequence":"first","affiliation":[{"name":"Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool L3 5RF, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5816-9146","authenticated-orcid":false,"given":"Kim-Kee","family":"Tan","sequence":"additional","affiliation":[{"name":"Tropical Infectious Diseases Research & Education Centre (TIDREC), Higher Institution Centre of Excellence (HICoE), Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1849-710X","authenticated-orcid":false,"given":"Amit","family":"Sinha","sequence":"additional","affiliation":[{"name":"New England Biolabs, Ipswich, Massachusetts, 01938, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nurul Aini","family":"Husin","sequence":"additional","affiliation":[{"name":"Tropical Infectious Diseases Research & Education Centre (TIDREC), Higher Institution Centre of Excellence (HICoE), Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2650-7518","authenticated-orcid":false,"given":"Fang Shiang","family":"Lim","sequence":"additional","affiliation":[{"name":"Tropical Infectious Diseases Research & Education Centre (TIDREC), Higher Institution Centre of Excellence (HICoE), Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7511-860X","authenticated-orcid":false,"given":"Shih Keng","family":"Loong","sequence":"additional","affiliation":[{"name":"Tropical Infectious Diseases Research & Education Centre (TIDREC), Higher Institution Centre of Excellence (HICoE), Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7305-0477","authenticated-orcid":false,"given":"Lesley","family":"Bell-Sakyi","sequence":"additional","affiliation":[{"name":"Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool L3 5RF, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4201-8367","authenticated-orcid":false,"given":"Clotilde K. 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