Coxiella Endosymbiont of Rhipicephalus microplus Modulates Tick Physiology With a Major Impact in Blood Feeding Capacity

Abstract

In the past decade, metagenomics studies exploring tick microbiota have revealed widespread interactions between bacteria and arthropods, including symbiotic interactions. Functional studies showed that obligate endosymbionts contribute to tick biology, affecting reproductive fitness and molting. Understanding the molecular basis of the interaction between ticks and their mutualist endosymbionts may help to develop control methods based on microbiome manipulation. Previously, we showed that Rhipicephalus microplus larvae with reduced levels of Coxiella endosymbiont of R. microplus (CERM) were arrested at the metanymph life stage (partially engorged nymph) and did not molt into adults. In this study, we performed a transcriptomic differential analysis of the R. microplus metanymph in the presence and absence of its mutualist endosymbiont. The lack of CERM resulted in an altered expression profile of transcripts from several functional categories. Gene products such as DA-P36, protease inhibitors, metalloproteases, and evasins, which are involved in blood feeding capacity, were underexpressed in CERM-free metanymphs. Disregulation in genes related to extracellular matrix remodeling was also observed in the absence of the symbiont. Taken together, the observed alterations in gene expression may explain the blockage of development at the metanymph stage and reveal a novel physiological aspect of the symbiont-tick-vertebrate host interaction.

Bacterial community of ticks (Acari: Ixodidae) and mammals from Arauca, Colombian Orinoquia

“…The results obtained of the ticks’ microbiome are consistent with previous studies in which bacteria of the family Coxiellaceae, encompassing Coxiella burnetii and Coxiella -like endosymbionts (CLEs), have been detected ( Wu-Chuang et al, 2021 ; Guizzo et al, 2022b ). Coxiella burnetii causes Q fever in humans and coxiellosis in animals, this distinction between C. burnetii and the Coxiella -like endosymbionts (CLEs) in ticks is problematic besides the latter are non-infectious to vertebrate hosts but are necessary for the health of these arthropods ( Duron et al, 2015 ; Brenner et al, 2021 ).…”

Ixodes ricinus ticks have a functional association with Midichloria mitochondrii

“…was eliminated ( Ben-Yosef et al., 2020 ). In R. microplus , the comparative transcriptomic analysis of Coxiella -free nymphs revealed a substantial under-expression of tick transcripts involved in their blood-feeding capacity ( Guizzo et al., 2022 ).…”

Diversity of midgut microbiota in ticks collected from white-tailed deer (Odocoileus virginianus) from northern Mexico

“…Members of the families Coxiellaceae and Francisellaceae with endosymbionts of the genera CLE and FLE were observed in R. microplus and D. nitens as previously described [ 25 ] in wild ticks from India, horse ticks, and livestock ticks from China [ 26 ]. Functional studies have shown that CLE contributes to tick biology by affecting reproductive fitness and molting [ 27 ]. Many Coxiella species have been recorded as endosymbionts in ticks; for example, in Amblyomma , their presence in the salivary glands alters the transmission of Ehrlichia chaffeensis [ 28 ].…”