A Coxiella mutualist symbiont is essential to the development of Rhipicephalus microplus

Abstract

The cattle tick Rhipicephalus microplus is a hematophagous ectoparasite that causes important economic losses in livestock. Different species of ticks harbor a symbiont bacterium of the genus Coxiella. It was showed that a Coxiella endosymbiont from R. microplus (CERM) is a vertically transmitted mutualist symbiont, comprising 98% of the 16S rRNA sequences in both eggs and larvae. Sequencing of the bacterial genome revealed genes for biosynthetic pathways for several vitamins and key metabolic cofactors that may provide a nutritional complement to the tick host. The CERM was abundant in ovary and Malpighian tubule of fully engorged female. Tetracycline treatment of either the tick or the vertebrate host reduced levels of bacteria in progeny in 74% for eggs and 90% for larvae without major impact neither on the reproductive fitness of the adult female or on embryo development. However, CERM proved to be essential for the tick to reach the adult life stage, as under antibiotic treatment no tick was able to progress beyond the metanymph stage. Data presented here suggest that interference in the symbiotic CERM-R. microplus relationship may be useful to the development of alternative control methods, highlighting the interdependence between ticks and their endosymbionts.

Comparison of closely related, uncultivated Coxiella tick endosymbiont population genomes reveals clues about the mechanisms of symbiosis

“…C. mudrowiae and CERM genomes show the loss of de novo synthesis of purines, but have retained the purine salvage pathway and the de novo pathway for synthesis of pyrimidines, consistent with what was reported previously for CRt (Gottlieb et al ., ). Conversely, all four CLE genomes have the coding capacity for cofactors and B vitamins (B7, B2, B6, B9, B5) that are typically lacking from blood‐meal restricted diets, such as thiamine and biotin (Smith et al ., ; Guizzo et al ., ).…”

“…The genome of CLE from the lone star tick, Amblyomma americanum (hereafter, referred as CLEAA), is only 657 kb (Smith et al, 2015), as opposed to the much larger genome of the CLE of Rhipicephalus microplus (hereafter referred as CERM), and CLE of Rhipicephalus turanicus (named Candidatus Coxiella mudrowiae, hereafter referred as CRt) which are 1.19 and 1.7 Mbp respectively. Despite their difference in size, as well as the distinct lifestyles of their tick hosts, CLEAA, CERM and CRt genomes encode complete pathways for the biosynthesis of several cofactors and vitamins, including those that produce folic acid, pyridoxine, lipoic acid, thiamine phosphate, biotin and riboflavin (Gottlieb et al, 2015;Smith et al, 2015;Guizzo et al, 2017). Although the production of several of these compounds could play an important role in establishing the symbiosis, direct proof of this remains essentially elusive.…”

“…Although the production of several of these compounds could play an important role in establishing the symbiosis, direct proof of this remains essentially elusive. Until today, and to the best of our knowledge, there are three attempts to experimentally test the effect of Coxiella on its tick host, showing substantial effects on host reproductive fitness and juvenile development when ticks were treated with antibiotics (Zhong et al, 2007;Guizzo et al, 2017;Zhang et al, 2017). However, the specific mechanism(s) underlining these effects is currently unknown, and hypotheses on possible functions essential for this symbiosis are based mostly on the available symbiont genomes.…”

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

“…Among arthropods, ticks (Arachnida: Ixodidae) are well known to engage in symbiotic associations with at least 10 different genera of maternally inherited bacteria (Ahantarig, Trinachartvanit, Baimai, & Grubhoffer, 2013;Duron et al, 2017). Ticks are specialized for an exclusive diet of vertebrate blood, and have evolved intimate interactions with beneficial symbionts that provide essential B vitamins and co-factors deficient in the blood diet (Bonnet, Binetruy, Hernández-Jarguín, & Duron, 2017;Duron et al, 2017Duron et al, , 2018Gerhart, Moses, & Raghavan, 2016;Gottlieb, Lalzar, & Klasson, 2015;Guizzo et al, 2017;Hunter et al, 2015;Olivieri et al, 2019;Smith, Driscoll, Gillespie, & Raghavan, 2015). Approximately two-thirds of tick species harbour Coxiella-like endosymbionts (hereafter Coxiella-LE), which are required for tick survival and reproduction (Gottlieb et al, 2015;Guizzo et al, 2017;Smith et al, 2015;Zhong, Jasinskas, & Barbour, 2007).…”

“…Ticks are specialized for an exclusive diet of vertebrate blood, and have evolved intimate interactions with beneficial symbionts that provide essential B vitamins and co-factors deficient in the blood diet (Bonnet, Binetruy, Hernández-Jarguín, & Duron, 2017;Duron et al, 2017Duron et al, , 2018Gerhart, Moses, & Raghavan, 2016;Gottlieb, Lalzar, & Klasson, 2015;Guizzo et al, 2017;Hunter et al, 2015;Olivieri et al, 2019;Smith, Driscoll, Gillespie, & Raghavan, 2015). Approximately two-thirds of tick species harbour Coxiella-like endosymbionts (hereafter Coxiella-LE), which are required for tick survival and reproduction (Gottlieb et al, 2015;Guizzo et al, 2017;Smith et al, 2015;Zhong, Jasinskas, & Barbour, 2007). Coxiella-LE genomes encode pathways for the biosynthesis of major B vitamins and co-factors that fit closely with the expected nutritional complements required for strict haematophagy (Gottlieb et al, 2015;Guizzo et al, 2017;Smith et al, 2015).…”