Stage- and host-dependent microbiome remodeling and reciprocal changes between Haemaphysalis longicornis and host skin

ABSTRACT Ticks harbor diverse microbial communities that are crucial for their biology and capacity to transmit pathogens. Although interactions between tick and host skin microbiomes are likely to play critical roles in feeding and pathogen transmission, these reciprocal changes during tick-host interactions remain largely unexplored. Here, we used 16S rRNA-seq to investigate how blood feeding by Haemaphysalis longicornis (larvae, nymphs, and adults) influences both the tick microbiome and the host skin microbiome. We further characterized microbial distribution across major tick tissues. Results revealed that feeding on different host species (mice vs rabbits) significantly altered the tick microbiome. Blood feeding reshaped microbial communities in the salivary glands and midgut, whereas the ovarian microbiome exhibited remarkable stability, suggesting the maintenance of a conserved symbiotic microbial core. Notably, Coxiella was identified as the dominant and stable bacterial symbiont across developmental stages and tissues and was consistently detected in eggs, suggesting that persistent vertical transmission may contribute to tick development, fitness, and nutritional homeostasis. On the other hand, Staphylococcus was consistently enriched at tick bite sites across host species and developmental stages, indicating that it may represent a key microbial responder involved in local microbiome remodeling and host skin responses to tick feeding. Collectively, these findings suggest that blood feeding drives dynamic remodeling of both tick and host skin-associated microbiomes and highlights Coxiella persistence and Staphylococcus enrichment as key microbial signatures of tick-host microbial interactions. Our study advances current understanding of microbiome cross-talk at the tick-host interface and provides new insights into microbiome-mediated mechanisms that may influence tick adaptation, host responses, and pathogen transmission. These findings also highlight potential opportunities for the development of microbiome-based strategies for the control of ticks and tick-borne diseases. IMPORTANCE Microbial communities are fundamental regulators of host physiology, development, and ecological interactions. In arthropod vectors, microbiomes play important roles in development, reproduction, and pathogen transmission. However, the dynamic interactions between vector-associated microbiomes and host skin microbiomes during blood feeding remain poorly understood, particularly in ticks. Here, we found that both tick-associated and host skin microbiomes showed stage- and host-dependent alterations following tick bites. Host species differentially reshaped microbial communities across tick tissues, whereas tick bites reciprocally altered the composition of host skin microbiomes. The stable vertical maintenance of Coxiella and the enrichment of Staphylococcus at bite sites suggest that specific microbial taxa might be involved in tick and host ecological interactions. Collectively, our findings provide evidence for bidirectional microbiome modulation at the tick-host interface and highlight potential targets for the development of microbiome-based strategies to control ticks and tick-borne diseases.