Abstract

Host-associated microbial dynamics are influenced by dietary and immune factors, but how exogenous microbial exposure shapes host-microbe dynamics remains poorly characterized. To investigate this phenomenon, we characterized the skin, rectum, and respiratory tract-associated microbiota in four aquarium-housed dolphins daily over a period of 6weeks, including administration of a probiotic during weeks 4 to 6. The environmental bacterial sources were also characterized, including the animals' human handlers, the aquarium air and water, and the dolphins' food supply. Continuous microbial exposure occurred between all sites, yet each environment maintained a characteristic microbiota, suggesting that the majority of exposure events do not result in colonization. Small changes in water physicochemistry had a significant but weak correlation with change in dolphin-associated bacterial richness but had no influence on phylogenetic diversity. Food and air microbiota were the richest and had the largest conditional influence on other microbiota in the absence of probiotics, but during probiotic administration, food alone had the largest influence on the stability of the dolphin microbiota. Our results suggest that respiratory tract and gastrointestinal epithelium interactions with air- and food-associated microbes had the biggest influence on host-microbiota dynamics, while other interactions, such as skin transmission, played only a minor role. Finally, direct oral stimulation with a foreign exogenous microbial source can have a profound effect on microbial stability. IMPORTANCE These results provide valuable insights into the ecological influence of exogenous microbial exposure, as well as laying the foundation for improving aquarium management practices. By comparing data for dolphins from aquaria that use natural versus artificial seawater, we demonstrate the potential influence of aquarium water disinfection procedures on dolphin microbial dynamics.

Highlights

  • Host-associated microbial dynamics are influenced by dietary and immune factors, but how exogenous microbial exposure shapes host-microbe dynamics remains poorly characterized

  • @cesarcardonau @gilbertjacka @shedd_aquarium proud to partner in one of a kind dolphin microbiome study showing the influence of probiotics and environmental interactions between the host and its diverse microbial communities msystems.asm.org 1 cantly different, while the microbial community composition of an individual host is remarkably stable over time [2]

  • Samples were collected over 42 consecutive days (24 September 2014 to 4 November 2014) in the Shedd Aquarium oceanarium, an indoor, temperature-controlled exhibit that uses recirculating artificial seawater

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Summary

Introduction

Host-associated microbial dynamics are influenced by dietary and immune factors, but how exogenous microbial exposure shapes host-microbe dynamics remains poorly characterized To investigate this phenomenon, we characterized the skin, rectum, and respiratory tract-associated microbiota in four aquariumhoused dolphins daily over a period of 6 weeks, including administration of a probiotic during weeks 4 to 6. The sources for aquarium-housed marine mammals, such as dolphins, are essentially limited to water, food, human handlers, and air, and in addition, they have a very stable diet. These animals, represent a useful model system in which to examine the influence of exogenous microbial exposure on the dynamics of host-associated microbial communities [14]. We hypothesized that the dolphin microbiota would exhibit an equilibrium with the regular environmental microbial exposure and that, if a foreign microbial exposure was administered, this would disturb host-associated microbial dynamics

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