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Title: Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics

Abstract

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 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,more » direct oral stimulation with a foreign exogenous microbial source can have a profound effect on microbial stability. IMPORTANCE Furthermore, 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.« less

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [4];  [5];  [2];  [5];  [6];  [7]
  1. Univ. of Chicago, Chicago, IL (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States)
  3. Illinois Inst. of Technology, Chicago, IL (United States)
  4. Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Illinois at Chicago, Chicago, IL (United States)
  5. John G. Shedd Aquarium, Chicago, IL (United States)
  6. Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Chicago, IL (United States)
  7. Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Science Foundation (NSF); John G. Shedd Aquarium; Argonne National Laboratory; USDOE
OSTI Identifier:
1489235
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 3; Journal Issue: 3; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; dolphin microbiome; environmental interactions; host microbiome; microbial ecology; microbial stability; probiotics

Citation Formats

Cardona, Cesar, Lax, Simon, Larsen, Peter, Stephens, Brent, Hampton-Marcell, Jarrad, Edwardson, Christian F., Henry, Chris, Van Bonn, Bill, Gilbert, Jack A., and Adams, Rachel I. Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics. United States: N. p., 2018. Web. doi:10.1128/mSystems.00052-18.
Cardona, Cesar, Lax, Simon, Larsen, Peter, Stephens, Brent, Hampton-Marcell, Jarrad, Edwardson, Christian F., Henry, Chris, Van Bonn, Bill, Gilbert, Jack A., & Adams, Rachel I. Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics. United States. doi:10.1128/mSystems.00052-18.
Cardona, Cesar, Lax, Simon, Larsen, Peter, Stephens, Brent, Hampton-Marcell, Jarrad, Edwardson, Christian F., Henry, Chris, Van Bonn, Bill, Gilbert, Jack A., and Adams, Rachel I. Tue . "Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics". United States. doi:10.1128/mSystems.00052-18. https://www.osti.gov/servlets/purl/1489235.
@article{osti_1489235,
title = {Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics},
author = {Cardona, Cesar and Lax, Simon and Larsen, Peter and Stephens, Brent and Hampton-Marcell, Jarrad and Edwardson, Christian F. and Henry, Chris and Van Bonn, Bill and Gilbert, Jack A. and Adams, Rachel I.},
abstractNote = {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 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. IMPORTANCE Furthermore, 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.},
doi = {10.1128/mSystems.00052-18},
journal = {mSystems},
issn = {2379-5077},
number = 3,
volume = 3,
place = {United States},
year = {2018},
month = {5}
}

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Cited by: 4 works
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Figures / Tables:

FIG 1 FIG 1: Overview of Shedd Aquarium microbial data. (A) Variations of Faith’s PD alpha diversity, food and air having significantly higher values than other sites and dolphin sites (chuff, rectum, and skin) having lower diversity values. (B) Weighted UniFrac beta diversity hierarchical clustering heat map shows how similar sites tendmore » to cluster together. (C) Weighted UniFrac NMDS plot of Shedd Aquarium samples. Dolphin sites aggregate by sample site rather than per individual, and they are clearly separated from each other. Nondolphin samples are much more intertwined, with air samples showing high similarities to dolphin skin, human hand, and nose, water, and food.« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.