Ear mite infection restructures otic microbial networks in conservation-reliant Santa Catalina Island foxes (Urocyon littoralis catalinae).

Abstract

Ceruminous gland tumours are highly prevalent in the ear canals of Santa Catalina Island foxes (Urocyon littoralis catalinae). Previous work suggests that tumours may result from a combination of ectoparasites, disruption of the host-associated microbiome, and host immunopathology. More specifically, ear mite infection has been associated with broad-scale microbial dysbiosis marked by secondary bacterial infection with the opportunistic pathogen Staphylococcus pseudintermedius. Together, ear mites and S. pseudintermedius probably sustain chronic inflammation and promote conditions suitable for tumour development. In the present study, we expanded upon this framework by constructing otic microbial community networks for mite-infected and uninfected foxes sampled in 2017-2019. Across sampling years, we observed consistent signatures of microbial dysbiosis in mite-infected ear canals, including reduced microbial diversity and shifted abundance towards S. pseudintermedius. Network analysis further revealed that mite infection disrupts overall community structure. In mite-infected networks, interaction strengths between taxa were generally weaker, and numerous subnetworks disappeared altogether. We also found that two strains of S. pseudintermedius connected to the main network, suggesting that multistrain biofilm formation may be occurring. In contrast, S. pseudintermedius is peripheral in the uninfected network, with its only connections including a second strain of S. pseudintermedius and the possible competitor Acinetobacter rhizosphaerae. Finally, the lineup of potential keystone taxa shifted across disease states. Fusobacteria spp., a carcinogenesis-promoting microbe, assumed a keystone role in the mite-infected community. Considered together, these findings provide insights into how mite infection may destabilize the microbiome and ultimately contribute to tumour development in this island endemic species.