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

Dietrich, Muriel; Kearney, Teresa; Seamark, Ernest C. J.; Paweska, Janusz T.; Markotter, Wanda

Phylogenetic analysis of saliva samples showed that the M. natalensis colony was infected with βand γ- HVs (figure 2c,d) , both genetically related to sequences detected in Miniopterus schreibersii in Spain [41] . By contrast, only β-HVs were detected in R. aegyptiacus (figure 2c). Sequences were embedded within a clade containing other fruit bat samples and were closely related to the only sequence available for R. aegyptiacus, obtained from a captive bat at the Budapest zoo in Hungary [42] . For both bat species, HV shedding prevalence varied strongly over time (GLM 3 : χ 2 2 = 8.848, p = 0.012, GLM 4 : χ 2 3 = 36.364, p < 0.001, figure 1b) and with age class (GLM 3 : χ 2 1 = 12.169, p < 0.001, GLM 4 : χ 2 1 = 3.913, p = 0.048). However, we found a distinct temporal pattern compared to Leptospira and AdV. Indeed, a peak of HV shedding was observed at the beginning of the reproductive season, followed by an almost twofold decrease in November for M. natalensis and a continuous decrease in October and January for R. aegyptiacus. The effect of age class was explained by the lower shedding prevalence that was observed in juveniles, suggesting the protection of juveniles by maternal antibodies during the first months of life. Additional sampling of R. aegyptiacus in April allowed us to observe a second peak of shedding (65 ± 10%), which may reflect the progressive loss of maternal protection and thus the infection of older juveniles. We also found that reproductive status was associated with an increase of HV shedding prevalence in R. aegyptiacus (GLM 4 : χ 2 1 = 6.028, p = 0.014), but this was probably driven by the absence of HV shedding in juveniles (thus in a non-reproductive state) in January compared to a shedding prevalence of 67% (± 24%) in lactating females at the same time (χ 2 1 = 16.944, p < 0.001). In females, pregnancy and lactating states were not associated to a different HV shedding prevalence compared to non-reproductive females. In males, although scrotal individuals always showed a higher HV shedding prevalence (100% in September, 85% in November) compared to the non-scrotal ones (77% and 46%, respectively), differences were not statistically significant. Overall, our results illustrate the HV temporal dynamics in bats, with similarity between two bat species. A notable aspect of HV infection is its latency, despite ongoing immunity, combined with the capacity to reactivate and spread to new hosts, especially during stress and pregnancy [43] [44] [45] . Moreover, male reproductive behaviours (such as biting) could be an important component of natural HV transmission, as shown in mice [46, 47] . Therefore, we could hypothesize that such factors may play an important role in favouring HV transmission at the beginning of the bat reproductive season.