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Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish

Prophylactic antibiotics in the aquaculture and ornamental fish industry are intended to prevent the negative impacts of disease outbreaks. Research in mice and humans suggests that antibiotics may disturb microbiome communities and decrease microbiome-mediated disease resistance, also known as “col...

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Autores principales: Schmidt, Victor, Gomez-Chiarri, Marta, Roy, Chelsea, Smith, Katherine, Amaral-Zettler, Linda
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5675916/
https://www.ncbi.nlm.nih.gov/pubmed/29124129
http://dx.doi.org/10.1128/mSystems.00133-17
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author Schmidt, Victor
Gomez-Chiarri, Marta
Roy, Chelsea
Smith, Katherine
Amaral-Zettler, Linda
author_facet Schmidt, Victor
Gomez-Chiarri, Marta
Roy, Chelsea
Smith, Katherine
Amaral-Zettler, Linda
author_sort Schmidt, Victor
collection PubMed
description Prophylactic antibiotics in the aquaculture and ornamental fish industry are intended to prevent the negative impacts of disease outbreaks. Research in mice and humans suggests that antibiotics may disturb microbiome communities and decrease microbiome-mediated disease resistance, also known as “colonization resistance.” If antibiotics impact fish as they do mice and humans, prophylactic administrations on aquaculture farms may increase downstream disease susceptibility in target hosts, despite short-term pathogen control benefits. We tested the effects of antibiotics on mortality after a pathogen challenge in the Poecilia sphenops black molly and subsequently tested if probiotic inoculations could reverse any antibiotic-induced losses of disease resistance. We found that antibiotic treatment significantly increased fish mortality. We further found that our two candidate probiotic bacterial species, Phaeobacter inhibens S4Sm and Bacillus pumilus RI06-95Sm, were able to colonize black molly microbiomes and reverse the negative impacts of antibiotics. Despite the positive impact on survival, probiotic treatment did not influence overall microbiome community structure or diversity. Our results suggest that subtle manipulations of microbiome composition can have dramatic impacts on host phenotype. The results of this study have implications for how antibiotic-treated microbiomes can be restored and suggest that small-scale additions may be as effective as wholesale transplants. IMPORTANCE Prophylactic antibiotics are widespread in the aquaculture industry and are used where vaccination is impossible or overly expensive. If antibiotics impact fish as they do mice and humans, prophylactic administrations in aquaculture and ornamental fish farms may increase downstream disease susceptibility in target hosts, despite short-term pathogen control benefits. Recent research has suggested that their use exacerbates bacterial outbreaks by creating sterile, nutrient-rich environments for invading pathogens to colonize and could help to explain rising economic costs of bacterial outbreaks in aquaculture. Our findings suggest a long-term cost of prophylactic antibiotic use and demonstrate a probiotic-based solution that does not rely on full microbiome community transplantation.
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spelling pubmed-56759162017-11-09 Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish Schmidt, Victor Gomez-Chiarri, Marta Roy, Chelsea Smith, Katherine Amaral-Zettler, Linda mSystems Research Article Prophylactic antibiotics in the aquaculture and ornamental fish industry are intended to prevent the negative impacts of disease outbreaks. Research in mice and humans suggests that antibiotics may disturb microbiome communities and decrease microbiome-mediated disease resistance, also known as “colonization resistance.” If antibiotics impact fish as they do mice and humans, prophylactic administrations on aquaculture farms may increase downstream disease susceptibility in target hosts, despite short-term pathogen control benefits. We tested the effects of antibiotics on mortality after a pathogen challenge in the Poecilia sphenops black molly and subsequently tested if probiotic inoculations could reverse any antibiotic-induced losses of disease resistance. We found that antibiotic treatment significantly increased fish mortality. We further found that our two candidate probiotic bacterial species, Phaeobacter inhibens S4Sm and Bacillus pumilus RI06-95Sm, were able to colonize black molly microbiomes and reverse the negative impacts of antibiotics. Despite the positive impact on survival, probiotic treatment did not influence overall microbiome community structure or diversity. Our results suggest that subtle manipulations of microbiome composition can have dramatic impacts on host phenotype. The results of this study have implications for how antibiotic-treated microbiomes can be restored and suggest that small-scale additions may be as effective as wholesale transplants. IMPORTANCE Prophylactic antibiotics are widespread in the aquaculture industry and are used where vaccination is impossible or overly expensive. If antibiotics impact fish as they do mice and humans, prophylactic administrations in aquaculture and ornamental fish farms may increase downstream disease susceptibility in target hosts, despite short-term pathogen control benefits. Recent research has suggested that their use exacerbates bacterial outbreaks by creating sterile, nutrient-rich environments for invading pathogens to colonize and could help to explain rising economic costs of bacterial outbreaks in aquaculture. Our findings suggest a long-term cost of prophylactic antibiotic use and demonstrate a probiotic-based solution that does not rely on full microbiome community transplantation. American Society for Microbiology 2017-11-07 /pmc/articles/PMC5675916/ /pubmed/29124129 http://dx.doi.org/10.1128/mSystems.00133-17 Text en Copyright © 2017 Schmidt et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Schmidt, Victor
Gomez-Chiarri, Marta
Roy, Chelsea
Smith, Katherine
Amaral-Zettler, Linda
Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
title Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
title_full Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
title_fullStr Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
title_full_unstemmed Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
title_short Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
title_sort subtle microbiome manipulation using probiotics reduces antibiotic-associated mortality in fish
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5675916/
https://www.ncbi.nlm.nih.gov/pubmed/29124129
http://dx.doi.org/10.1128/mSystems.00133-17
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