Affiliation:
1. Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool L3 5RF, UK
2. Tropical Infectious Diseases Research & Education Centre (TIDREC), Higher Institution Centre of Excellence (HICoE), Universiti Malaya, Kuala Lumpur 50603, Malaysia
3. New England Biolabs, Ipswich, Massachusetts, 01938, USA
Abstract
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.
Funder
Newton Fund
Ministry of Higher Education, Malaysia
UK Biotechnology and Biological Sciences Research Council
Wellcome Trust
Marie Skłodowska Curie Grant
New England Biolabs
Cited by
2 articles.
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