Ixodes ricinus tick bacteriome alterations based on a climatically representative survey in Hungary

Abstract

ABSTRACT The microbial communities of disease vectors may represent a key feature in several biological functions and thus deserve special attention in light of climate change and the consequent need to develop novel control strategies. Nevertheless, vector-borne microbial networks are still poorly understood. Assessing vectors’ microbial interactions and climatic dependencies may contribute to better estimating pathogen transmission characteristics and public health risks. In a climatically representative country-wide survey, Ixodes ricinus ticks were collected from 17 locations in Hungary. Using shotgun metagenomic sequencing, the bacteriome composition was analyzed by investigating the relationship between the abundance of nymphs and females in various climatic environments. Bacterial composition on the genus level revealed a significant difference between the samples from females and nymphs. Within the core bacteriome, females and nymphs showed significant variation in the following genera: Arsenophonus, Bacillus, Candidatus Midichloria, Rhodococcus, Sphingomonas, Staphylococcus, and Wolbachia. Among females, according to temperature strata, the following were found differentiating: Curtobacterium, Pseudomonas, and Sphingomonas. There was no genus with a significant difference in precipitation categories for females. Curtobacterium showed significant variation between temperature and Bacillus and Curtobacterium for various precipitation levels in the nymphs. The composition of vector-borne bacteriome members showed significant alterations at sampling points with different climatic conditions and development stages of the tick hosts. Our findings not only pave the way toward understanding tick-borne bacterial networks and interdependencies but also shed light on the high potential for the presence of a possible biological tick control species, the tick parasitoid, Ixodiphagus hookeri based on related bacteriome patterns. IMPORTANCE Climate-sensitive disease vectors, such as ticks, respond to the environment with changes in their microbiome. These changes can affect the emergence or re-emergence of various vector-borne pathogens, such as the causative agent of Lyme borreliosis (LB) or tick-borne encephalitis. This aspect is particularly emphasized in light of climate change. The climatically representative assessment of microbiome differences in various developmental stages of the most common Central European tick species, Ixodes ricinus, deepens our understanding of the potential climatic factors behind microbial relative abundance and interaction changes. This knowledge can support the development of novel disease vector control strategies.

Keywords

• Ixodes ricinus
• bacteriome
• climate
• female
• nymph