Evolutionary changes in symbiont community structure in ticks

Abstract

Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

“…Nevertheless, FLE and other bacterial endosymbionts have been known to colonize salivary glands, and their presence in this organ does not ensure transmission to vertebrate hosts (41). Similar observations have been made for other hard ticks and their obligatory symbionts (36,40), suggesting a potential nutritional role of the symbionts in supplying B vitamins missing in the tick blood meal (11,42).…”

“…Also, the distance between FLE from H. aegyptium and H. marginatum corresponds to that shown in studies from Hungary, Ethiopia, and Yemen (9,10,29), indicating that FLE strains are comparable in different locations. Congruence between host and symbiont phylogenies has been shown for many obligatory symbiosis systems where the association is required to support the dietary needs of the host (35), and it was also shown for Rhipicephalus and Coxiella-like endosymbiont lineages (36). The FLE sequences of Hyalomma are close to an FLE sequence from Amblyomma maculatum which was hypothesized to have recently evolved from pathogenic Francisella species (37).…”

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

“…Symbionts—i.e., microorganisms engaged in close and long-term interactions with their tick hosts—are exceptionally diverse in ticks: at least 10 distinct genera of maternally-inherited bacteria have been reported in ticks over the last decade (listed in Table 1 and Figure 2) (Duron et al, 2017). Three of these symbionts are only found in ticks: Coxiella -LE, which infects at least two thirds of tick species, Midichloria , which inhabits the mitochondria of some tick species, and Francisella -LE, which has only been reported in a few tick species (Table 1).…”

“…Less well studied or understood are whole microbial communities hosted by ticks, which attract much less attention, yet are equally important. These communities include TBP, but also non-pathogenic microorganisms such as commensal and mutualistic microbes that are also abundant in ticks (Andreotti et al, 2011; Carpi et al, 2011; Williams-Newkirk et al, 2014; Duron et al, 2015a, 2017). Until recently, these non-pathogenic microorganisms were generally overlooked by scientists working with ticks and TBP.…”

“…This knowledge is of both medical and veterinary interest since it may enable the reassessment of tick-associated health risks, but also of ecological and evolutionary importance by highlighting co-evolutionary processes acting between ticks and their microbes. Indeed, some symbionts, but not all (Weller et al, 1998), have a joint evolutionary history of several million years with their tick hosts (Almeida et al, 2012; Duron et al, 2017), suggesting that complex interactions may have evolved in these associations. If biologists aim to fully understand the ecological and evolutionary processes involved in tick biology and the emergence of tick-borne diseases, a thorough examination of non-pathogenic microorganisms is also required.…”