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

A significant effect of reproductive condition was found in the saliva of R. aegyptiacus, with the composition of oral microbiota being different between pregnant and non-pregnant adult females (PERMANOVA: p = 0.026). For example, LEfSe analysis revealed that salivary microbiota of pregnant females was enriched with Actinobacillus and Streptococcus. In contrast, no significant difference was observed in the saliva of M. natalensis females (analyses were not performed for faeces and urine because of the limited sample size for non-pregnant females). The effect of reproductive condition in males was tested in R. aegyptiacus only, as no scrotal males were caught in the M. natalensis colony, but we found no significant difference of salivary microbiota composition between scrotal and non-scrotal adult males (PERMANOVA: p = 0.707). Such a relationship between female reproductive condition and microbiota composition has already been reported in South American bats [20] , and is consistent with findings in humans showing that the gut microbiota is altered by pregnancy [50] . Shift of microbiota composition in reproductive females was evidenced in M. natalensis, in which, parturient and post-lactating females had completely distinct microbiotas for the three body habitats (PERMANOVAs: all p < 0.01, figure 5 ). Indeed, microbiota of parturient females were enriched in Staphylococcus and Corynebacterium in all body habitats, while diverse phylotypes were associated with the post-lactating status, such as Streptococcus in faeces, Haemophilus in saliva and members of Planctomycetaceae in urine. It is likely that the overall immune modulation during pregnancy plays a role in alteration of the microbiota [51] . Surprisingly, in R. aegyptiacus, no significant difference was found in salivary microbiota composition between pregnant and lactating females (PERMANOVA: p = 0.75). One explanation could be that the two bat species were not sampled at exactly the same reproductive stages and that shift of microbiota was probably stage-dependent. For example, Collado et al. [52] have reported extreme changes in microbiota from the first to the third trimester of pregnancy in women, while others have shown some stability over the perinatal period [53] . Therefore, it is crucial to consider the time frame and reproductive stages sampled. Overall, our results showed that a general shift in microbiota composition may occur in reproductive female bats, but further studies are needed to determine whether the processes are similar to what is observed in humans [51] .