Abstract

The Pacific coast tick, Dermacentor occidentalis Marx, is found throughout California and can harbor agents that cause human diseases such as anaplasmosis, ehrlichiosis, tularemia, Rocky Mountain spotted fever and rickettsiosis 364D. Previous studies have demonstrated that nonpathogenic endosymbiotic bacteria can interfere with Rickettsia co-infections in other tick species. We hypothesized that within D. occidentalis ticks, interference may exist between different nonpathogenic endosymbiotic or nonendosymbiotic bacteria and Spotted Fever group Rickettsia (SFGR). Using PCR amplification and sequencing of the rompA gene and intergenic region we identified a cohort of SFGR-infected and non-infected D. occidentalis ticks collected from San Diego County. We then amplified a partial segment of the 16S rRNA gene and used next-generation sequencing to elucidate the microbiomes and levels of co-infection in the ticks. The SFGR R. philipii str. 364D and R. rhipicephali were detected in 2.3% and 8.2% of the ticks, respectively, via rompA sequencing. Interestingly, next generation sequencing revealed an inverse relationship between the number of Francisella-like endosymbiont (FLE) 16S rRNA sequences and Rickettsia 16S rRNA sequences within individual ticks that is consistent with partial interference between FLE and SFGR infecting ticks. After excluding the Rickettsia and FLE endosymbionts from the analysis, there was a small but significant difference in microbial community diversity and a pattern of geographic isolation by distance between collection locales. In addition, male ticks had a greater diversity of bacteria than female ticks and ticks that weren’t infected with SFGR had similar microbiomes to canine skin microbiomes. Although experimental studies are required for confirmation, our findings are consistent with the hypothesis that FLEs and, to a lesser extent, other bacteria, interfere with the ability of D. occidentalis to be infected with certain SFGR. The results also raise interesting possibilities about the effects of putative vertebrate hosts on the tick microbiome.

Highlights

  • The Pacific Coast tick, Dermacentor occidentalis Marx ( D. occidentalis) is the most widely distributed tick in California and is found in chaparral and shrubland areas from northern Baja California to California and Oregon (Furman & Loomis, 1984)

  • While the precise mechanism of the bacterial interactions need elucidation, our results suggest that carriage of certain pathogenic Spotted Fever group Rickettsia (SFGR) in ticks could be modulated by other non-rickettsial endosymbionts, providing a potential non-chemical alternative to SFGR control

  • No ticks were positive for Francisella tularensis, 39 ticks (8.2%) were positive for R. rhipicephali and 12 (2.3%) were positive for R. philipii 364D as identified by sequencing of the rompA gene and intergenic region (IGR)

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Summary

Introduction

The Pacific Coast tick, Dermacentor occidentalis Marx ( D. occidentalis) is the most widely distributed tick in California and is found in chaparral and shrubland areas from northern Baja California to California and Oregon (Furman & Loomis, 1984). D. occidentalis is a three-host, hard-shell tick that feeds on a variety of vertebrates, such as rodents, rabbits, cattle, deer, horses and humans. Surveys of this tick have shown its ability to vector human pathogens such as Francisella tularensis (tularemia), Coxiella burnetii (Q fever), Anaplasma phagocytophilum (human granulocytic anaplasmosis), Ehrlichia chaffeensis (human monocytic ehrlichiosis), Rickettsia rickettsii (Rocky Mountain spotted fever, RMSF) and Rickettsia philipii 364D (hereafter R. philipii) as well as the non-pathogenic spotted fever group Rickettsia, R. rhipicephali (Parker, Brooks & Marsh, 1929; Cox, 1940; Lane et al, 1981; Holden et al, 2003; Wikswo et al, 2008; Shapiro et al, 2010). Discovered in 1966, and long suspected of being able to cause disease, it was only recently confirmed to be associated with eschars and lymphadenopathy in people at the site of a tick bite (Lane et al, 1981; Shapiro et al, 2010; Johnston et al, 2013)

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