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.
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DOI:
10.1099/mgen.0.001045
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发表时间:
2023-07
期刊:
影响因子:
3.9
通讯作者:
Khoo, Jing Jing
Khoo, Jing Jing
中科院分区:
生物学2区
文献类型:
--
作者:
Beliavskaia, Alexandra;Tan, Kim -Kee;Sinha, Amit;Husin, Nurul Aini;Lim, Fang Shiang;Loong, Shih Keng;Bell-Sakyi, Lesley;Carlow, Clotilde K. S.;AbuBakar, Sazaly;Darby, Alistair C.;Makepeace, Benjamin L.;Khoo, Jing Jing

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虽然跳蚤通常被简单地认为是一种叮咬滋扰和过敏性皮炎的原因,但它们是世界范围内重要的疾病媒介,特别是细菌性人畜共患病,如鼠疫(由啮齿动物跳蚤传播)和一些立克次体病和巴尔通体病。世界性的猫(Ctenocephalides felis)和狗(Ctenocephalides canis)跳蚤,以及Ctenocephalides orientis(仅限于热带和亚热带亚洲),在人类住所繁殖,是猫抓热(由 巴尔通体 spp.)和 立克次 spp.,包括 猫立克次体 (蚤传斑疹热病原体)及 阿森本立克次体,疑似病原体。这些 立克次 spp.是一个系统发育分支的成员,称为“过渡组”,其中包括人类病原体和节肢动物特异性内共生体。相对分散的跳蚤微生物组还可以含有其他内共生体,包括各种各样的微生物。 Wolbachia 菌株在这里,我们提出了两个C。东方病原体(巴尔通体 和 R. asembonensis)从马来西亚,一本小说 Wolbachia 菌株(wCori)和C. orientis线粒体;所有均通过跳蚤组织直接宏基因组测序获得。此外,我们还分离出两个 Wolbachia 马来西亚C.猫蜱细胞培养和回收的环化基因组组件,其中之一(wCfeF是新测序的。我们证明,这三个 Wolbachia 菌株代表不同的主要进化枝(“超群”),其中两个似乎是跳蚤特异性的。这些 Wolbachia 基因组表现出与生殖寄生或互利共生相关的特征的独特组合,包括原噬菌体WO、细胞质不相容因子和专性细胞内微生物的生物素操纵子。第一个圆形组件, R.阿森邦内斯 包括与公开的质粒相比具有显著不同的结构和基因含量的质粒;此外,这种新型质粒也在来自美国的猫蚤宏基因组中检测到。在过渡组的正选择下的基因座分析揭示了参与宿主-病原体相互作用的基因,这可能有助于宿主转换。最后,第一个 B。克拉里奇亚科 与来自其他大陆的分离株相比,来自亚洲的基因组表现出大规模的基因组稳定性,除了预测介导与脊椎动物宿主相互作用的区域中的SNP。这些研究结果突出了关于栉首虫相关细菌基因组多样性的数据的缺乏,并提出了关于跳蚤微生物组成员之间的相互作用如何影响载体能力的问题。
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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