Rickettsial pathogens drive microbiota assembly in Hyalomma marginatum and Rhipicephalus bursa ticks

Abstract

Most tick-borne pathogens (TBPs) are secondarily acquired by ticks during feeding on infected hosts, which imposes 'priority effect' constraints, as arrival order influences the establishment of new species in a microbial community. Here we tested whether once acquired, TBPs contribute to bacterial microbiota functioning by increasing community stability. For this, we used Hyalomma marginatum and Rhipicephalus bursa ticks collected from cattle in different locations of Corsica and combined 16S rRNA amplicon sequencing and co-occurrence network analysis, with high-throughput pathogen detection, and in silico removal of nodes to test for impact of rickettsial pathogens on network properties. Despite its low centrality, Rickettsia showed preferential connections in the networks, notably with a keystone taxon in H. marginatum, suggesting facilitation of Rickettsia colonisation by the keystone taxon. In addition, conserved patterns of community assembly in both tick species were affected by Rickettsia removal, suggesting that privileged connections of Rickettsia in the networks make this taxon a driver of community assembly. However, Rickettsia removal had minor impact on the conserved 'core bacterial microbiota' of H. marginatum and R. bursa.Interestingly, networks of the two tick species with Rickettsia have similar node centrality distribution, a property that is lost after Rickettsia removal, suggesting that this taxon drives specific hierarchical interactions between bacterial microbes in the microbiota. The study indicates that tick-borne Rickettsia play a significant role in the tick bacterial microbiota, despite their low centrality. These bacteria are influential and contribute to the conservation of the 'core bacterial microbiota' while also promoting community stability.

Spatial patterns ofHyalomma marginatum-borne pathogens in the Occitanie region (France), a focus on the intriguing dynamics ofRickettsia aeschlimannii

“…These results are consistent with previous studies performed on H. marginatum in southern France which reported high infection rates; from 75% in individual ticks in H. marginatum collected around the French Mediterranean sea between 2016 and 2019 (Bernard et al 2024) to 100% of the pools of H. marginatum in Corsica (Grech-Angelini et al 2020). Such high infection rates observed in our study and many others (Maitre et al 2023; Bernard et al 2024) raise the question of the pathogenic status of this detected Rickettsia, since a high number of human patients suffering from rickettsiosis should be observed, but reported cases remain extremely rare and only imported cases have been reported in France to date. While Grech-Angelini et al (2020) suggested that human exposure to R. aeschlimannii infection in Corsica is high and human cases of tick-borne spotted fever acquired in Corsica could often be due to R. aeschlimannii , there is no information available for its vectorial competence based on experimental approaches, showing that this assumption must be nuanced.…”

“…Indeed, the transovarian transmission of R. aeschlimannii in H. marginatum paired with its high infection rates both support this assumption (Parola, Paddock, and Raoult 2005;Azagi et al 2017). In the literature, such hypothesis have already been suggested for H. marginatum (Maitre et al 2023;Boularias et al 2021). Tick symbionts are typically classified as primary or secondary symbionts, depending on their role in the tick's survival.…”

Dynamic nesting of Anaplasma marginale in the microbial communities of Rhipicephalus microplus

“…bursa ticks, suggesting it acts as a community assembly driver (Maitre et al, 2023). Conversely, in R. microplus, infection by the protozoan Theileria sp.…”

“…Temporal changes in the vector microbiome may affect the ability of pathogens to persist in vectors, transmit to hosts, and cause disease, as the transmission of vector-borne pathogens often involves complex interactions between pathogens and the microbiome (Abraham et al, 2017;Maitre et al, 2022Maitre et al, , 2023Narasimhan et al, 2014Narasimhan et al, , 2017. While the studies by Krawczyk et al (2022), and Lejal et al (2021) provided valuable insights into the dynamic nature of symbiont-microbiome interactions and the temporal dynamics of TBPs within questing ticks, it is essential to acknowledge a crucial limitation inherent to this sampling approach.…”

Exploring the impact of breast cancer on colonization resistance of mouse microbiota using network node manipulation

“…Network analysis is a powerful tool that allows researchers to investigate the complex interactions and associations between different microbial taxa within a community [ 8 , 9 ]. By constructing co-occurrence networks based on correlations between microbial abundances, researchers can gain insights into the structure, organization, and stability of the microbial community [ 10 , 11 ].…”