Wastewater treatment works change the intestinal microbiomes of insectivorous bats

Abstract

Mammals, born with a near-sterile intestinal tract, are inoculated with their mothers' microbiome during birth. Thereafter, extrinsic and intrinsic factors shape their intestinal microbe assemblage. Wastewater treatment works (WWTW), sites synonymous with pollutants and pathogens, receive influent from domestic, agricultural and industrial sources. The high nutrient content of wastewater supports abundant populations of chironomid midges (Diptera), which transfer these toxicants and potential pathogens to their predators, such as the banana bat Neoromicia nana (Vespertilionidae), thereby influencing their intestinal microbial assemblages. We used next generation sequencing and 16S rRNA gene profiling to identify and compare intestinal bacteria of N. nana at two reference sites and two WWTW sites. We describe the shared intestinal microbiome of the insectivorous bat, N. nana, consisting of seven phyla and eleven classes. Further, multivariate analyses revealed that location was the most significant driver (sex, body size and condition were not significant) of intestinal microbiome diversity. Bats at WWTW sites exhibited greater intestinal microbiota diversity than those at reference sites, likely due to wastewater exposure, stress and/or altered diet. Changes in their intestinal microbiota assemblages may allow these bats to cope with concomitant stressors.

Fig 1. Locality map of wastewater treatment works (WWTW) and reference sites, KwaZulu-Natal, South Africa.

Red squares represent WWTWs and green squares represent reference sites. Sites are the same as those used in [36].

Fig 2. NMDS plots for the intestinal bacterium phyla in Neoromicia nana caught at wastewater treatment works (WWTW) and reference sites in KwaZulu-Natal, South Africa.

(A) Individuals grouped by site (B = Buffelsdrift, I = Inkunzi, V = Verulam, U = Umbilo). (B) Individuals grouped by sex (M = Male, F = Female).

Fig 3

The total number of intestinal bacterial phyla (A), classes (B), orders (C), families (D) and genera (E) in Neoromicia nana caught at wastewater treatment works (WWTW) and reference sites in KwaZulu-Natal, South Africa. Green = Inkunzi, Blue = Buffelsdrift, Red = Umbilo WWTW and Orange = Verulam WWTW.

Fig 4. The average relative abundance of intestinal bacterium phyla in Neoromicia nana caught at wastewater treatment works (WWTW) and reference sites in KwaZulu-Natal, South Africa.

“Other” includes OTUs not assigned to a phylum.