Bacterial microbiota composition of Ixodes ricinus ticks: the role of environmental variation, tick characteristics and microbial interactions

Abstract

Ecological factors, host characteristics and/or interactions among microbes may all shape the occurrence of microbes and the structure of microbial communities within organisms. In the past, disentangling these factors and determining their relative importance in shaping within-host microbiota communities has been hampered by analytical limitations to account for (dis)similar environmental preferences (‘environmental filtering’). Here we used a joint species distribution modelling (JSDM) approach to characterize the bacterial microbiota of one of the most important disease vectors in Europe, the sheep tick Ixodes ricinus, along ecological gradients in the Swiss Alps. Although our study captured extensive environmental variation along elevational clines, the explanatory power of such large-scale ecological factors was comparably weak, suggesting that tick-specific traits and behaviours, microhabitat and -climate experienced by ticks, and interactions among microbes play an important role in shaping tick microbial communities. Indeed, when accounting for shared environmental preferences, evidence for significant patterns of positive or negative co-occurrence among microbes was found, which is indicative of competition or facilitation processes. Signals of facilitation were observed primarily among human pathogens, leading to co-infection within ticks, whereas signals of competition were observed between the tick endosymbiont Spiroplasma and human pathogens. These findings highlight the important role of small-scale ecological variation and microbe-microbe interactions in shaping tick microbial communities and the dynamics of tick-borne disease.

Temporal patterns inIxodes ricinusmicrobial communities: an insight into tick-borne microbe interactions

“…Competition for the same niche might explain the negative correlations observed between these two groups of Borrelia. However, these findings contrast with those presented in Aivelo et al [19] as positive correlations were detected between the relapsing fever spirochete B. miyamotoi with Rickettsiella and two Borrelia species belonging to the group Borrelia Lyme borreliosis (B. garinii, B. afzelii). Because clinical co-infections with several TBPs are commonly reported [104][105][106] and are known to affect both disease symptoms and severity [107,108], it will be crucial to determine conditions in which Borrelia RF and Borrelia LB would be in competition or on the contrary could collaborate and thus coinfect ticks.…”

“…Furthermore, the fact that not all these studies used negative controls to identify potential contaminating OTUs and remove them from their datasets calls for caution in attempts to draw conclusions about these differences, particularly when we know that these OTUs can represent more than 50% of sequences detected in tick samples [22]. [6,12,16,18,19], were identified as bacteria present in the environment [57][58][59][60][61][62]. While very few of the above mentioned references reported performing negative controls while studying tick microbiota [12,19], it is important to keep in mind that some of these genera could also correspond to contaminants that may arise during extraction or amplification steps [22,30,[63][64][65].…”

“…[6,12,16,18,19], were identified as bacteria present in the environment [57][58][59][60][61][62]. While very few of the above mentioned references reported performing negative controls while studying tick microbiota [12,19], it is important to keep in mind that some of these genera could also correspond to contaminants that may arise during extraction or amplification steps [22,30,[63][64][65]. Here, the dataset underwent a thorough contaminant filtering, based on negative control composition [22], decreasing in this way the risk that these OTUs correspond to contaminants.…”

“…The fact that Rickettsia were positively correlated with a maternally inherited bacteria is particularly surprising, especially because members of this genus have been frequently reported to be involved in antagonist relationships with symbiotic or pathogenic genera [9,10,19,[100][101][102][103]. This potential complementarity between these two genera will have to deepen in the future by characterizing the bacterial transcriptome or metabolome of ticks infected with these bacteria alone or in association.…”

“…The microbiota of several tick species of the genera Ixodes, Dermacentor, Haemaphysalis, Rhipicephalus and Amblyomma has been studied (see in [15]) and all these works have given crucial details on microbial communities in ticks and improved our knowledge on tick microbial community ecology. However, few information are currently available on the microbiota composition of the tick Ixodes ricinus [6,12,[16][17][18][19][20][21][22], the predominant tick species in western Europe, able to transmit the largest variety of pathogens, including the Lyme disease agent Borrelia burgdorferi s.l.. Moreover, several of these previous I. ricinus microbiota analyses may have overestimated the microbiota diversity due to extraction step contamination and the lack of controls in their analysis [22].…”