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Review
. 2017 Jun 8:7:236.
doi: 10.3389/fcimb.2017.00236. eCollection 2017.

The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission

Affiliations
Review

The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission

Sarah I Bonnet et al. Front Cell Infect Microbiol. .

Abstract

Ticks are among the most important vectors of pathogens affecting humans and other animals worldwide. They do not only carry pathogens however, as a diverse group of commensal and symbiotic microorganisms are also present in ticks. Unlike pathogens, their biology and their effect on ticks remain largely unexplored, and are in fact often neglected. Nonetheless, they can confer multiple detrimental, neutral, or beneficial effects to their tick hosts, and can play various roles in fitness, nutritional adaptation, development, reproduction, defense against environmental stress, and immunity. Non-pathogenic microorganisms may also play a role in driving transmission of tick-borne pathogens (TBP), with many potential implications for both human and animal health. In addition, the genetic proximity of some pathogens to mutualistic symbionts hosted by ticks is evident when studying phylogenies of several bacterial genera. The best examples are found within members of the Rickettsia, Francisella, and Coxiella genera: while in medical and veterinary research these bacteria are traditionally recognized as highly virulent vertebrate pathogens, it is now clear to evolutionary ecologists that many (if not most) Coxiella, Francisella, and Rickettsia bacteria are actually non-pathogenic microorganisms exhibiting alternative lifestyles as mutualistic ticks symbionts. Consequently, ticks represent a compelling yet challenging system in which to study microbiomes and microbial interactions, and to investigate the composition, functional, and ecological implications of bacterial communities. Ultimately, deciphering the relationships between tick microorganisms as well as tick symbiont interactions will garner invaluable information, which may aid in the future development of arthropod pest and vector-borne pathogen transmission control strategies.

Keywords: microbial interactions; microbiome; tick; tick borne pathogens; tick symbionts.

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Figures

Figure 1
Figure 1
Origin and acquisition of tick microorganisms. Red arrows: vertebrate pathogens acquired from tick bites; blue arrows: maternally inherited tick symbionts acquired via transovarial and transtadial transmission; green arrows: microorganisms acquired from the environment.
Figure 2
Figure 2
Simplified eubacterial phylogeny showing the evolutionary relationships between the ten genera containing maternally inherited tick symbionts (labeled 1–10, as detailed in Table 1).
Figure 3
Figure 3
Evolutionary relationships between pathogenic and non-pathogenic (symbiotic) forms within the Francisella, Coxiellai, and Rickettsia bacterial genera. (A–C) Simplified phylogenies of Coxiella, Francisella, and Rickettsia, respectively, adapted from Perlman et al. (2006), Weinert et al. (2009), Duron et al. (2015a), and Sjodin et al. (2012). Red: pathogenic forms; blue: endosymbiotic forms associated with arthropods (ticks for Francisella and Coxiella; ticks and other arthropods for Rickettsia); black: bacterial outgroups. Colored circles on tree branches indicate major evolutionary transitions from symbiotic ancestors to pathogenic descendants (red circles) and from pathogenic ancestors to symbiotic descendants (blue circles).

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