Molecular prevalence and genetic diversity of Bartonella spp. in stray cats of İzmir, Turkey

Köseoğlu, Ahmet Efe; Can, Hüseyin; Güvendi, Mervenur; Karakavuk, Muhammet; Manyatsi, Pumla Bhekiwe; Alak, Sedef Erkunt; Döşkaya, Aysu Değirmenci; Gül, Aytül; Döşkaya, Mert; Gürüz, Adnan Yüksel; Ün, Cemal

doi:10.1186/s13071-022-05431-3

“…The final component of the C. orientis microbiome sequenced here, B. clarridgeiae, has been detected frequently in Ctenocephalides spp. fleas and the blood or other tissues of cats and dogs worldwide [25, 130–132], with a number of reports across South-East Asia [133–136], although to the best of our knowledge no confirmed zoonotic infections from this part of the world have been documented. However, only two other genomes are available (one complete and circularized [14]), which are derived from feline blood isolates from France and the USA.…”

Section: Discussionmentioning

confidence: 99%

Metagenomics of culture isolates and insect tissue illuminate the evolution of Wolbachia, Rickettsia and Bartonella symbionts in Ctenocephalides spp. fleas

Beliavskaia

¹

,

Tan

²

,

Sinha

³

et al. 2023

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While fleas are often perceived simply as a biting nuisance and a cause of allergic dermatitis, they represent important disease vectors worldwide, especially for bacterial zoonoses such as plague (transmitted by rodent fleas) and some of the rickettsioses and bartonelloses. The cosmopolitan cat (Ctenocephalides felis) and dog (Ctenocephalides canis) fleas, as well as Ctenocephalides orientis (restricted to tropical and subtropical Asia), breed in human dwellings and are vectors of cat-scratch fever (caused by Bartonella spp.) and Rickettsia spp., including Rickettsia felis (agent of flea-borne spotted fever) and Rickettsia asembonensis , a suspected pathogen. These Rickettsia spp. are members of a phylogenetic clade known as the ‘transitional group’, which includes both human pathogens and arthropod-specific endosymbionts. The relatively depauperate flea microbiome can also contain other endosymbionts, including a diverse range of Wolbachia strains. Here, we present circularized genome assemblies for two C. orientis-derived pathogens ( Bartonella clarridgeiae and R. asembonensis ) from Malaysia, a novel Wolbachia strain (wCori), and the C. orientis mitochondrion; all were obtained by direct metagenomic sequencing of flea tissues. Moreover, we isolated two Wolbachia strains from Malaysian C. felis into tick cell culture and recovered circularized genome assemblies for both, one of which (wCfeF) is newly sequenced. We demonstrate that the three Wolbachia strains are representatives of different major clades (‘supergroups’), two of which appear to be flea-specific. These Wolbachia 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 R. asembonensis 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–pathogen interactions that may facilitate host switching. Finally, the first B. clarridgeiae 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 Ctenocephalides-associated bacteria and raise questions regarding how interactions between members of the flea microbiome might influence vector competence.

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“…The final component of the C. orientis microbiome sequenced here, B. clarridgeiae , has been detected frequently in Ctenocephalides spp. fleas and the blood or other tissues of cats and dogs worldwide [17, 123-125], with a number of reports across South-East Asia [126-129], although to the best of our knowledge no confirmed zoonotic infections from this part of the world have been documented. However, only two other genomes are available (one complete and circularised [130]), which are derived from feline blood isolates from France and the USA.…”

Section: Discussionmentioning

confidence: 99%

Metagenomics of culture isolates and insect tissue illuminate the evolution ofWolbachia,RickettsiaandBartonellasymbionts inCtenocephalidesspp. fleas

Beliavskaia

¹

,

Tan

²

,

Sinha

³

et al. 2023

Preprint

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While fleas are often perceived simply as a biting nuisance and cause of allergic dermatitis, they represent important disease vectors worldwide, especially for bacterial zoonoses such as plague (transmitted by rodent fleas) and some of the rickettsioses and bartonelloses. The cosmopolitan cat (Ctenocephalidesfelis) and dog (C. canis) fleas, as well asC. orientis(restricted to tropical and subtropical Asia), breed in human dwellings and are vectors of cat-scratch fever (caused byBartonellaspp.) andRickettsiaspp. of the so-called "transitional group". The latter includesR. felis(agent of flea-borne spotted fever) andR. asembonensis, an emerging pathogen. The relatively depauperate flea microbiome can also contain arthropod-specific endosymbionts, including a diverse range ofWolbachiastrains. Here, we present circularized genome assemblies for twoC. orientis-associated pathogens (Bartonella clarridgeiaeandR. asembonensis) from Malaysia, a novelWolbachiastrain (wCori), and theC. orientismitochondrion; all obtained by direct metagenomic sequencing of flea tissues. Moreover, we isolated twoWolbachiastrains from MalaysianC. felisinto tick cell culture and recovered circularized genome assemblies for both, one of which (wCfeF) is newly sequenced. We demonstrate that the threeWolbachiastrains are representatives of different major clades ("supergroups"), two of which appear to be flea-specific. TheseWolbachiagenomes 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 forR. asembonensisincludes 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 US. Analysis of loci under positive selection in the transitional group revealed genes involved in host-pathogen interactions that may facilitate host switching. Finally, the firstB. clarridgeiaegenome from Asia exhibited largescale 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 ofCtenocephalides-associated bacteria and raise questions regarding how interactions between members of the flea microbiome might influence vector competence.

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“…Due to limited knowledge and awareness, CSD can affect both pet owners and those without pets ( Stull et al, 2012 ). The prevalence of bartonellosis has been documented worldwide which included saliva of the domestic cat (10.9 %), domestic cats (34.3 %), the veterinary worker population (37.1 %), vampire bats (67 %), and stray cats (45 %) ( Oskouizadeh et al, 2010 , Müller et al, 2017 , Oteo et al, 2017 , Becker et al, 2018 , Köseoğlu et al, 2022 ). Thousands of pet owners in the United States and Europe report Bartonella infection annually, with many requiring hospitalization ( Chomel et al, 2006 ).…”

Section: Introductionmentioning

confidence: 99%

Epidemiology of feline bartonellosis and molecular characteristics of Bartonella henselae in Bangladesh

Kabir,

Shaker Chouhan,

Habib

et al. 2024

Saudi Journal of Biological Sciences

0

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Molecular prevalence and genetic diversity of Bartonella spp. in stray cats of İzmir, Turkey

Cited by 10 publications

References 49 publications

Metagenomics of culture isolates and insect tissue illuminate the evolution of Wolbachia, Rickettsia and Bartonella symbionts in Ctenocephalides spp. fleas

Metagenomics of culture isolates and insect tissue illuminate the evolution of Wolbachia, Rickettsia and Bartonella symbionts in Ctenocephalides spp. fleas

Metagenomics of culture isolates and insect tissue illuminate the evolution ofWolbachia,RickettsiaandBartonellasymbionts inCtenocephalidesspp. fleas

Epidemiology of feline bartonellosis and molecular characteristics of Bartonella henselae in Bangladesh

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