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

ABSTRACT 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 know...

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Autores principales:	Victor Schmidt, Marta Gomez-Chiarri, Chelsea Roy, Katherine Smith, Linda Amaral-Zettler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	antibiotics aquaculture Bacillus colonization resistance microbial ecology microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7e309d09f4cb420285a4d41b9b2bcae2
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spelling	oai:doaj.org-article:7e309d09f4cb420285a4d41b9b2bcae22021-12-02T19:45:29ZSubtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish10.1128/mSystems.00133-172379-5077https://doaj.org/article/7e309d09f4cb420285a4d41b9b2bcae22017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00133-17https://doaj.org/toc/2379-5077ABSTRACT 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.Victor SchmidtMarta Gomez-ChiarriChelsea RoyKatherine SmithLinda Amaral-ZettlerAmerican Society for MicrobiologyarticleantibioticsaquacultureBacilluscolonization resistancemicrobial ecologymicrobiomeMicrobiologyQR1-502ENmSystems, Vol 2, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	antibiotics aquaculture Bacillus colonization resistance microbial ecology microbiome Microbiology QR1-502
spellingShingle	antibiotics aquaculture Bacillus colonization resistance microbial ecology microbiome Microbiology QR1-502 Victor Schmidt Marta Gomez-Chiarri Chelsea Roy Katherine Smith Linda Amaral-Zettler Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish
description	ABSTRACT 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.
format	article
author	Victor Schmidt Marta Gomez-Chiarri Chelsea Roy Katherine Smith Linda Amaral-Zettler
author_facet	Victor Schmidt Marta Gomez-Chiarri Chelsea Roy Katherine Smith Linda Amaral-Zettler
author_sort	Victor Schmidt
title	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_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_sort	subtle microbiome manipulation using probiotics reduces antibiotic-associated mortality in fish
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/7e309d09f4cb420285a4d41b9b2bcae2
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Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish

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