Synchronized shift of oral, faecal and urinary microbiotas in bats and natural infection dynamics during seasonal reproduction

Abstract

Seasonal reproduction is a period of extreme physiological and behavioural changes, yet we know little about how it may affect host microbial communities (i.e. microbiota) and pathogen transmission. Here, we investigated shifts of the bacterial microbiota in saliva, urine and faeces during the seasonal reproduction of bats in South Africa, and test for an interaction in shedding patterns of both bacterial (Leptospira) and viral (adeno- and herpesviruses) agents. Based on a comparative approach in two cave-dwelling bat species and high-throughput sequencing of the 16S rRNA gene, we demonstrated a clear signature in microbiota changes over the reproduction season, consistent across the multiple body habitats investigated, and associated with the sex, age and reproductive condition of bats. We observed in parallel highly dynamic shedding patterns for both bacteria and viruses, but did not find a significant association between viral shedding and bacterial microbiota composition. Indeed, only Leptospira shedding was associated with alterations in both the diversity and composition of the urinary microbiota. These results illustrate how seasonal reproduction in bats substantially affects microbiota composition and infection dynamics, and have broad implications for the understanding of disease ecology in important reservoir hosts, such as bats.In part by the National Research Foundation (NRF) of South Africa: the NRF-DST South African Research Chair held by Prof Markotter, grant no. 98339, as well as grant numbers 92524, 85756 and 91496, and grant UID 78566 (NRF RISP grant for the ABI3500). This research was partially supported by the Cooperative Agreement Number [5 NU2GGH001874-02-00], funded by the Centers for Disease Control and Prevention, USA. M.D.’s postdoctoral fellowship was funded by a Capacity Building Grant from the National Research Foundation, South Africa (grant no. UID 92524).http://rsos.royalsocietypublishing.orgam2018Centre for Wildlife ManagementMammal Research InstituteMedical Virolog