Patterns of viral communities and the host–pathogen interactions with ecological factors in bat caves

Abstract

Abstract Background Bats (Chiroptera) are major sources of epidemics. To understand the dynamics of diseases, it is crucial to study the dynamics of microorganisms in the environment and the relationship between microorganisms and bats. In this study, we investigated the soil virus communities in bat caves using viral metagenomic sequencing technology. We further explored host–pathogen interactions with regard to the effects of the environment by combining analyses of microorganisms (viruses and bacteria) and immune genes (major histocompatibility complex, MHC) of the main resident species (Rhinolophus ferrumequinum) in the bat caves. Results A total of 31 families of viruses were identified. Significant differences were observed in alpha diversity, beta diversity, and the relative abundances of soil virus families, indicating their habitat specificity in bat caves. Zoonotic risk viruses were also found, and the composition of viruses in bat caves was similar to the distribution of virus families of R. ferrumequinum in a previous study. Second, the alpha diversity of both viruses and bacteria was significantly negatively correlated with precipitation of the wettest month. The relative abundances of viral and bacterial families were correlated with MHC allele frequencies. Moreover, a structural equation model further revealed that the precipitation of the coldest quarter significantly negatively affected virus diversity, which in turn significantly negatively affected the MHC allele frequencies in R. ferrumequinum. The MHC allele frequencies were negatively affected by bacterial alpha diversity. Conclusions The results of the present study suggest that the polymorphism of the MHC class I gene of R. ferrumequinum is driven by environmental pathogen selection pressure and that environmental climate affects the host immune genes by regulating the diversity of microorganisms. This study is the first to demonstrate the diversity of virus communities in bat caves, and thus has significance for protecting bat habitats from human disturbance and in preventing zoonotic diseases.