Temporal patterns in Ixodes ricinus microbial communities: an insight into tick-borne microbe interactions

Abstract

Background Ticks transmit pathogens of medical and veterinary importance and are an increasing threat to human and animal health. Assessing disease risk and developing new control strategies requires identifying members of the tick-borne microbiota as well as their temporal dynamics and interactions. Methods Using high-throughput sequencing, we studied the Ixodes ricinus microbiota and its temporal dynamics. 371 nymphs were monthly collected during three consecutive years in a peri-urban forest. After a Poisson lognormal model was adjusted to our data set, a principal component analysis, sparse network reconstruction, and differential analysis allowed us to assess seasonal and monthly variability of I. ricinus microbiota and interactions within this community. Results Around 75% of the detected sequences belonged to five genera known to be maternally inherited bacteria in arthropods and to potentially circulate in ticks: Candidatus Midichloria, Rickettsia, Spiroplasma, Arsenophonus and Wolbachia. The structure of the I. ricinus microbiota varied over time with interannual recurrence and seemed to be mainly driven by OTUs commonly found in the environment. Total network analysis revealed a majority of positive partial correlations. We identified strong relationships between OTUs belonging to Wolbachia and Arsenophonus, evidence for the presence of the parasitoid wasp Ixodiphagus hookeri in ticks. Other associations were observed between the tick symbiont Candidatus Midichloria and pathogens belonging to Rickettsia. Finally, more specific network analyses were performed on TBP-infected samples and suggested that the presence of pathogens belonging to the genera Borrelia, Anaplasma and Rickettsia may disrupt microbial interactions in I. ricinus. Conclusions We identified the I. ricinus microbiota and documented marked shifts in tick microbiota dynamics over time. Statistically, we showed strong relationships between the presence of specific pathogens and the structure of the I. ricinus microbiota. We detected close links between some tick symbionts and the potential presence of either pathogenic Rickettsia or a parasitoid in ticks. These new findings pave the way for the development of new strategies for the control of ticks and tick-borne diseases.

Recently Evolved Francisella-Like Endosymbiont Outcompetes an Ancient and Evolutionarily Associated Coxiella-Like Endosymbiont in the Lone Star Tick (Amblyomma americanum) Linked to the Alpha-Gal Syndrome

“…Both Rhizobiaceae and Xanthobacteraceae are nonresident, opportunistic bacteria that ticks acquire from their environment ( Sun et al., 2000 ; Scoles, 2004 ; Andreotti et al., 2011 ; Carpi et al., 2011 ; Institute of Medicine (US) Committee on Lyme Disease and Other Tick-Borne Diseases, 2011 ; Ponnusamy et al., 2014 ; Clayton et al., 2015 ; Galili, 2016 ; Gurfield et al., 2017 ). Lejal and colleagues (2021) detected a significant abundance of a Rhizobiaceae-Multi_1 in Rickettsia- positiv e I. ricinus ticks, suggesting a completely different observation of our findings that Rhizobiaceae was negatively correlated with the Rickettsiaceae, but positively correlated with Coxiellaceae. This finding could present a potential interaction between known bacterial endosymbionts and possible environmental bacteria transiently acquired by ticks.…”

“…maculatum ticks. Lejal et al. (2021) also identified a substantial prevalence of CMM in I. ricinus ticks that were positive with bacteria in the Rickettsia genus.…”

Co-occurrence networks reveal more complexity than community composition in resistance and resilience of microbial communities

“…We analyzed networks for each period and treatment separately, following previous studies 61 – 64 , to assure > 25 communities per network 65 . Thus, the drought-period network was based on 36 communities (6 plots * 6 time points) and the rewetting period network was based on 48 communities (6 plots * 8 time points).…”

Assessing Temporal Changes in Microbial Communities in Hyalomma dromedarii Collected From Camels in the UAE Using High-Throughput Sequencing

“…Tick symbionts also affect pathogen colonization and transmission to the vertebrate host, for instance, FLEs have favored the establishment of Francisella novicida in Dermacentor andersoni ( 27 ). On the other hand, Rickettsia is a maternally inherited bacterium in arthropods and was found previously in a study on temporal patterns of microbial communities in Ixodes ricinus ( 23 ). Rickettsia occurs in nature as endosymbionts and pathogens.…”

“…Microbes that cohabit the midgut of a tick could affect host fitness and its competence (ability to transmit a pathogen) ( 20 ). The ecological relationships among these microorganisms may be ranging from beneficial to detrimental ( 21 ) resulting in suppression or enhancement of some microbial species ( 22 , 23 ). Furthermore, these interactions between the microbiota and pathogens are essential to understand because the tick microbiota may sway pathogen colonization and its transmission to the vertebrate host ( 24 ).…”