A Coxiella-Like Endosymbiont Is a Potential Vitamin Source for the Lone Star Tick

Abstract

Amblyomma americanum (Lone star tick) is an important disease vector in the United States. It transmits several human pathogens, including the agents of human monocytic ehrlichiosis, tularemia, and southern tick-associated rash illness. Blood-feeding insects (Class Insecta) depend on bacterial endosymbionts to provide vitamins and cofactors that are scarce in blood. It is unclear how this deficiency is compensated in ticks (Class Arachnida) that feed exclusively on mammalian blood. A bacterium related to Coxiella burnetii, the agent of human Q fever, has been observed previously within cells of A. americanum. Eliminating this bacterium (CLEAA, Coxiella-like endosymbiont of A. americanum) with antibiotics reduced tick fecundity, indicating that it is an essential endosymbiont. In an effort to determine its role within this symbiosis, we sequenced the CLEAA genome. While highly reduced (656,901 bp) compared with C. burnetii (1,995,281 bp), the CLEAA genome encodes most major vitamin and cofactor biosynthesis pathways, implicating CLEAA as a vitamin provisioning endosymbiont. In contrast, CLEAA lacks any recognizable virulence genes, indicating that it is not a pathogen despite its presence in tick salivary glands. As both C. burnetii and numerous “Coxiella-like bacteria” have been reported from several species of ticks, we determined the evolutionary relationship between the two bacteria. Phylogeny estimation revealed that CLEAA is a close relative of C. burnetii, but was not derived from it. Our results are important for strategies geared toward controlling A. americanum and the pathogens it vectors, and also contribute novel information regarding the metabolic interdependencies of ticks and their nutrient-provisioning 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 ., ).…”

Coxiella Detection in Ticks from Wildlife and Livestock in Malaysia

“…These findings suggest that the role of the Coxiella -like bacteria or endosymbiont may not be equally important across all tick species. Since the bulk of current studies into the physiological role of Coxiella endosymbiosis in ticks are investigated in A. americanum , extra precautions must be exercised when extrapolating the findings to other tick species (Klyachko et al 2007, Zhong et al 2007, Smith et al 2015). …”

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

“…By replacing the ancestral Coxiella ‐LE, the novel symbiont colonizes a pre‐adapted tick physiological environment that requires the provision of vitamin B: thus, it must be able to synthesize these compounds as with the ancestral Coxiella ‐LE. The presence of several vitamin B biosynthesis pathways is ancestral in the genera Coxiella and Francisella , and all members of these genera, including pathogenic species that are also all intracellular, have conserved these abilities through their radiation (Duron et al, ; Gerhart et al, ; Meibom & Charbit, ; Rowe & Huntley, ; van Schaik, Chen, Mertens, Weber, & Samuel, ; Smith et al, ): all Francisella ‐LE and Coxiella ‐LE are already pre‐adapted to nutritional symbioses with ticks. Beyond B vitamins, the replacement of ancestral Coxiella ‐LE suggests that the new symbiont could supply an additional benefit that the ancestral Coxiella ‐LE was unable to supply to ticks, thereby out‐competing them.…”