Sex-Specific Linkages Between Taxonomic and Functional Profiles of Tick Gut Microbiomes

Ticks transmit the most diverse array of disease agents and harbor one of the most diverse microbial communities. Major progress has been made in the characterization of the taxonomic profiles of tick microbiota. However, the functional profiles of tick microbiome have been comparatively less studied. In this proof of concept we used state-of-the-art functional metagenomics analytical tools to explore previously reported datasets of bacteria found in male and female Ixodes ovatus, Ixodes persulcatus, and Amblyomma variegatum. Results showed that both taxonomic and functional profiles have differences between sexes of the same species. KEGG pathway analysis revealed that male and female of the same species had major differences in the abundance of genes involved in different metabolic pathways including vitamin B, amino acids, carbohydrates, nucleotides, and antibiotics among others. Partial reconstruction of metabolic pathways using KEGG enzymes suggests that tick microbiome form a complex metabolic network that may increase microbial community resilience and adaptability. Linkage analysis between taxonomic and functional profiles showed that among the KEGG enzymes with differential abundance in male and female ticks only 12% were present in single bacterial genera. The rest of these enzymes were found in more than two bacterial genera, and 27% of them were found in five up to ten bacterial genera. Comparison of bacterial genera contributing to the differences in the taxonomic and functional profiles of males and females revealed that while a small group of bacteria has a dual-role, most of the bacteria contribute only to functional or taxonomic differentiation between sexes. Results suggest that the different life styles of male and female ticks exert sex-specific evolutionary pressures that act independently on the phenomes (set of phenotypes) and genomes of bacteria in tick gut microbiota. We conclude that functional redundancy is a fundamental property of male and female tick microbiota and propose that functional metagenomics should be combined with taxonomic profiling of microbiota because both analyses are complementary.