Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics

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...

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Autores principales:	Cesar Cardona, Simon Lax, Peter Larsen, Brent Stephens, Jarrad Hampton-Marcell, Christian F. Edwardson, Chris Henry, Bill Van Bonn, Jack A. Gilbert
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	dolphin microbiome environmental interactions host microbiome microbial ecology microbial stability probiotics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/99e3bd06ce104b929cd1ba3aa0481cfc
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spelling	oai:doaj.org-article:99e3bd06ce104b929cd1ba3aa0481cfc2021-12-02T18:39:15ZEnvironmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics10.1128/mSystems.00052-182379-5077https://doaj.org/article/99e3bd06ce104b929cd1ba3aa0481cfc2018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00052-18https://doaj.org/toc/2379-5077ABSTRACT 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 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.Cesar CardonaSimon LaxPeter LarsenBrent StephensJarrad Hampton-MarcellChristian F. EdwardsonChris HenryBill Van BonnJack A. GilbertAmerican Society for Microbiologyarticledolphin microbiomeenvironmental interactionshost microbiomemicrobial ecologymicrobial stabilityprobioticsMicrobiologyQR1-502ENmSystems, Vol 3, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	dolphin microbiome environmental interactions host microbiome microbial ecology microbial stability probiotics Microbiology QR1-502
spellingShingle	dolphin microbiome environmental interactions host microbiome microbial ecology microbial stability probiotics Microbiology QR1-502 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
description	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 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.
format	article
author	Cesar Cardona Simon Lax Peter Larsen Brent Stephens Jarrad Hampton-Marcell Christian F. Edwardson Chris Henry Bill Van Bonn Jack A. Gilbert
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
publishDate	2018
url	https://doaj.org/article/99e3bd06ce104b929cd1ba3aa0481cfc
work_keys_str_mv	AT cesarcardona environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT simonlax environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT peterlarsen environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT brentstephens environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT jarradhamptonmarcell environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT christianfedwardson environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT chrishenry environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT billvanbonn environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics AT jackagilbert environmentalsourcesofbacteriadifferentiallyinfluencehostassociatedmicrobialdynamics
_version_	1718377751695589376

Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics

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