Metatranscriptomics provide insights into the role of the symbiont Midichloria mitochondrii in Ixodes ticks

Ticks are important vectors of bacterial, viral, and protozoan pathogens of humans and animals worldwide. Candidatus Midichloria mitochondrii is a highly abundant bacterial endosymbiont found in many tick species, including two medically important ticks respectively found in Europe and Australia, Ixodes ricinus and Ixodes holocyclus. The present study aimed to determine the symbiont's biological role by identifying lateral gene transfer (LGT) events, characterizing the transcriptome, and performing differential expression analyses. Metatranscriptomic data revealed that M. mitochondrii species in I. ricinus and I. holocyclus were equipped with the metabolic potential and were actively transcribing the genes for several important roles including heme, biotin and folate synthesis, oxidative stress response, osmotic regulation, and ATP production in microaerobic conditions. Differential expression analyses additionally showed an upregulation in stringent response and DNA repair genes in M. mitochondrii of I. holocyclus nymphs compared to adults. Low rates of differential expression suggest the symbiont may lack global gene regulation, as observed in other endosymbionts. Moreover, the identification of an LGT event and the proposed specialization of the M. mitochondrii strains, mIxholo1 and mIxholo2, for different I. holocyclus life stages highlight the complex interactions between M. mitochondrii and their tick hosts.