Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics

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 i...

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Main Authors: Cesar Cardona, Simon Lax, Peter Larsen, Brent Stephens, Jarrad Hampton-Marcell, Christian F. Edwardson, Chris Henry, Bill Van Bonn, Jack A. Gilbert
Format: Article
Language:English
Published: American Society for Microbiology 2018-05-01
Series:mSystems
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00052-18
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spelling doaj-7c010a10abef42e49f47260cf915e8262020-11-25T02:42:01ZengAmerican Society for MicrobiologymSystems2379-50772018-05-0133e00052-1810.1128/mSystems.00052-18Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial DynamicsCesar CardonaSimon LaxPeter LarsenBrent StephensJarrad Hampton-MarcellChristian F. EdwardsonChris HenryBill Van BonnJack A. GilbertThese 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.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 6 weeks, 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.https://doi.org/10.1128/mSystems.00052-18dolphin microbiomeenvironmental interactionshost microbiomemicrobial ecologymicrobial stabilityprobiotics
collection DOAJ
language English
format Article
sources DOAJ
author Cesar Cardona
Simon Lax
Peter Larsen
Brent Stephens
Jarrad Hampton-Marcell
Christian F. Edwardson
Chris Henry
Bill Van Bonn
Jack A. Gilbert
spellingShingle Cesar Cardona
Simon Lax
Peter Larsen
Brent Stephens
Jarrad Hampton-Marcell
Christian F. Edwardson
Chris Henry
Bill Van Bonn
Jack A. Gilbert
Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
mSystems
dolphin microbiome
environmental interactions
host microbiome
microbial ecology
microbial stability
probiotics
author_facet Cesar Cardona
Simon Lax
Peter Larsen
Brent Stephens
Jarrad Hampton-Marcell
Christian F. Edwardson
Chris Henry
Bill Van Bonn
Jack A. Gilbert
author_sort Cesar Cardona
title Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
title_short Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
title_full Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
title_fullStr Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
title_full_unstemmed Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
title_sort environmental sources of bacteria differentially influence host-associated microbial dynamics
publisher American Society for Microbiology
series mSystems
issn 2379-5077
publishDate 2018-05-01
description 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.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 6 weeks, 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.
topic dolphin microbiome
environmental interactions
host microbiome
microbial ecology
microbial stability
probiotics
url https://doi.org/10.1128/mSystems.00052-18
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