Genome sequencing of Coxiella endosymbionts from Dermacentor marginatus and Ornithodoros maritimus

Coxiella burnetii is a parasitic intracellular bacterium firstly isolated from a tick. It causes Q fever, a zoonotic disease in humans. Its symptoms range from asymptomatic to flu-like and endocarditis when chronic. C. burnetii can develop inside phagolysosomes from different hosts and presents a biphasic cycle with both active and resistance forms. The latter can persist for long periods in the environment and is the primary infective form. Several Coxiella-like endosymbionts (Coxiella-LEs) phylogenetically related to C. burnetii have been described as nutritional mutualists of ticks. Their relationship questioned if C. burnetii parasitic status evolved from a mutualistic symbiont by gaining different virulence factors or its ancestor was already a parasite. We sequenced two new Coxiella-LE genomes the hard tick Dermacentor marginatus and the sof tick Ornithodoros maritimus. The latter being a close C. burnetii relative. We conducted a comparative genomic and phylogenetic analysis using those newly obtained Coxiella-LE and 40 Coxiellaceae genomes from five genera: Aquicella, Berkiella, Rickettsiella, Diplorickettsia, and Coxiella (including several environmental representatives). All Coxiella representatives can produce B vitamins and co-factors while the other Coxiellaceae present lower metabolic potential. The Dot/Imc T4 Secretion System is generally present among all Coxiellaceae. In C. burnetii it is part of a pathogenic island lost or inactivated in Coxiella-LEs. Hence, the ancestor of C. burnetii and Coxiella-LE was a parasitic symbiont able to produce vitamins and cofactors and manipulate its hosts. C. burnetii lineage acquired laterally a Sha antiporter that could have some role in the resistance form as it is involved in alkali resistance and sporulation in other bacteria.