Ticks convert pathogenicCoxiellainto endosymbionts

Abstract

Both symbiotic and pathogenic bacteria in the family Coxiellaceae cause morbidity and mortality in humans and animals. For instance, Coxiella-like endosymbionts (CLEs) improve the reproductive success of ticks — a major disease vector, while Coxiella burnetii is the etiological agent of human Q fever and uncharacterized coxiellae cause infections in both animals and humans. To better understand the evolution of pathogenesis and symbiosis in this group of intracellular bacteria, we sequenced the genome of a CLE present in the soft tick Ornithodoros amblus (CLEOA) and compared it to the genomes of other bacteria in the order Legionellales. Our analyses confirmed that CLEOA is more closely related to C. burnetii, the human pathogen, than to CLEs in hard ticks, and showed that most clades of CLEs contain both endosymbionts and pathogens, indicating that several CLE lineages have evolved independently from pathogenic Coxiella. We also determined that the last common ancestor of CLEOA and C. burnetii was equipped to infect macrophages, and that even though HGT contributed significantly to the evolution of C. burnetii, most acquisition events occurred primarily in ancestors predating the CLEOA-C. burnetii divergence. These discoveries clarify the evolution of C. burnetii, which previously was assumed to have emerged when an avirulent tick endosymbiont recently gained virulence factors via HGT. Finally, we identified several metabolic pathways, including heme biosynthesis, that are likely critical to the intracellular growth of the human pathogen but not the tick symbiont, and show that the use of heme analogs is a promising approach to controlling C. burnetii infections.

The Prevalence of Coxiella burnetii in Hard Ticks in Europe and Their Role in Q Fever Transmission Revisited—A Systematic Review

“…The main survival strategy of CLE is the vertical transmission via the egg, but also horizontal transfer, possibly via co-feeding, was proven (156,157). Recent results based on genome sequencing have shown that certain CLEs seem to have evolved from an ancestor capable of infection of immune cells (158). Hence, a loss of pathogenic potential was suggested.…”

“…Novel tick-borne pathogens are emerging, and as the evolution of C. burnetii is closely linked to endosymbionts, the possibility of other Coxiella spp. being pathogenic should not be neglected, considering that bird infections or human skin infections were reported (38,49,103,158). Increasing the knowledge on evolutionary processes and the pathogenic potential of CLE could likewise also contribute to a better understanding of the epidemiology of C. burnetii.…”

Differential microbial composition in parasitic vs. questing ticks based on 16S next-generation sequencing

“…in cases (Raulf et al, 2018). Other bacteria of notable prevalence are Coxiella and Francisella, which have been reported to exist symbiotically in ticks such as Rickettsia-like, Coxiella-like, and Francisella-like endosymbiont (Song et al, 2022), and potentially play a crucial role in tick development by supplying B vitamins (Brenner et al, 2021). Networks show the interrelationship between bacteria and Supplementary Tables 6, 7 present the detailed correlation results of groups.…”