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

Abstract

Mutualistic interactions with microbes have facilitated the adaptation of major eukaryotic lineages to restricted diet niches. Hence, ticks with their strictly blood‐feeding lifestyle are associated with intracellular bacterial symbionts through an essential B vitamin supplementation. In this study, examination of bacterial diversity in 25 tick species of the genus Amblyomma showed that three intracellular bacteria, Coxiella‐like endosymbionts (LE), Francisella‐LE and Rickettsia, are remarkably common. No other bacterium is as uniformly present in Amblyomma ticks. Almost all Amblyomma species were found to harbour a nutritive obligate symbiont, Coxiella‐LE or Francisella‐LE, that is able to synthesize B vitamins. However, despite the co‐evolved and obligate nature of these mutualistic interactions, the structure of microbiomes does not mirror the Amblyomma phylogeny, with a clear exclusion pattern between Coxiella‐LE and Francisella‐LE across tick species. Coxiella‐LE, but not Francisella‐LE, form evolutionarily stable associations with ticks, commonly leading to co‐cladogenesis. We further found evidence for symbiont replacements during the radiation of Amblyomma, with recent, and probably ongoing, invasions by Francisella‐LE and subsequent replacements of ancestral Coxiella‐LE through transient co‐infections. Nutritional symbiosis in Amblyomma ticks is thus not a stable evolutionary state, but instead arises from conflicting origins between unrelated but competing symbionts with similar metabolic capabilities.

Ticks convert pathogenicCoxiellainto endosymbionts

“…Tick endosymbionts are ephemeral. Phylogenies of only a few CLEs are congruent with those of their hosts (Duron et al 2017;Binetruy et al 2020), probably because older CLEs get replaced by newer CLEs derived from distantly-related coxiellae. In a similar fashion, FLEs seem to have replaced older CLEs in several tick lineages (Gerhart et al 2016(Gerhart et al , 2018Duron et al 2017Duron et al , 2018b).…”

“…Gaining new symbionts via horizontal transmission could also protect ticks from becoming dependent on a degraded endosymbiont. While the mechanistic details of this process are not understood, phylogenetic patterns of CLE and FLE distribution strongly indicate the occurrence of horizontal transmission of bacteria between ticks (Gerhart et al 2016(Gerhart et al , 2018Duron et al 2017;Binetruy et al 2020). It is not clear whether there is direct tick-to-tick transfer or whether unrelated ticks acquire similar bacteria from common environmental sources (Duron et al 2018a).…”

“…For instance, CLEs in A. americanum and A. sculptum have highly reduced (~0.60 Mbp) genomes that are similar in size to Buchnera, which established its symbiosis with aphids more than 200 million years ago (Moran et al 1993). Putting all this information together, it appears that a combination of vertical inheritance, horizontal transmission, and periodic replacement of old symbionts with new pathogen-derived symbionts underlies the complex distribution pattern of endosymbionts observed in ticks (Gottlieb et al 2015;Smith et al 2015;Gerhart et al 2016Gerhart et al , 2018Duron et al 2017;Tsementzi et al 2018;Binetruy et al 2020).…”

Sequence of aCoxiellaendosymbiont of the tickAmblyomma nuttallisuggests a pattern of convergent genome reduction in theCoxiellagenus

“…Clade C displays a good degree of co-cladogenesis with Rhipicephalus hosts, while CEs of two unrelated clades (B and D) were found in Amblyomma hosts (Duron et al 2015). Interestingly, the known clade B Amblyomma hosts came from the African continent, while clade D hosts are American (Duron et al 2015; Binetruy et al 2020). Currently, genomes of representatives of three of the four Coxiella clades have been sequenced, i.e.…”

Assessing biosynthetic gene cluster diversity in a multipartite nutritional symbiosis between herbivorous turtle ants and conserved gut symbionts

“…Among mutualistic bacteria the nutritional symbionts supplement a large diversity of nutrients to the diet of their insect hosts which often rely on nutritionally limited food sources. In the case of strictly blood-sucking ticks, intracellular bacterial symbionts provide vitamin B to the host 3,4 . Xylophagous termites rely on a diverse community of gut bacteria to degrade the lignocellulose from wood and also fix nitrogen for their hosts.…”