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

Tuomas Aivelo,Barbara Tschirren,Anna Norberg

doi:10.7717/peerj.8217

Tuomas Aivelo, Barbara Tschirren + Show 1 more

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https://doi.org/10.7717/peerj.8217

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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.

Highlights

Introduction1998, Rigaud et al 2010, Sofonea et al 2015)
Microbial communities within organisms consist of symbionts, commensals, mutualists and pathogens that co-occur simultaneously and potentially influence each other (Petney and Andrews1998, Rigaud et al 2010, Sofonea et al 2015)
We used a joint species distribution modelling (JSDM) framework to quantify the relative importance of large scale, site-level environmental variables, tick-level characteristics and interactions among microbes in shaping tick microbiota composition along elevational gradients in the Swiss Alps

Summary

Introduction

1998, Rigaud et al 2010, Sofonea et al 2015) These microbial communities may be shaped by a range of factors and processes, including the environment, host and microbe genetics and the occurrence and abundance of other microbial species (Adair and Douglas 2017). The host’s immune system can influence colonization success of microbes (Hawley and Altizer 2011), with cross-immunity preventing the colonization of different microbes with similar antigenic properties (Durand et al 2015). Direct interactions among microbes might affect colonization, or replication success after colonization, through competition or facilitation processes. Competition may occur when different microbes use the same, limited resources within a host (Lello et al 2004), whereas facilitation may occur directly through the production of public goods (West and Buckling 2003) or indirectly through the modification of the host’s physiology (Abraham et al 2017) or immune defense (Rodríguez et al 1999)

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