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Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees

Widespread antibiotic usage in apiculture contributes substantially to the global dissemination of antimicrobial resistance and has the potential to negatively influence bacterial symbionts of honey bees (Apis mellifera). Here, we show that routine antibiotic administration with oxytetracycline sele...

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Autores principales: Daisley, Brendan A., Pitek, Andrew P., Chmiel, John A., Gibbons, Shaeley, Chernyshova, Anna M., Al, Kait F., Faragalla, Kyrillos M., Burton, Jeremy P., Thompson, Graham J., Reid, Gregor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7519052/
https://www.ncbi.nlm.nih.gov/pubmed/32978472
http://dx.doi.org/10.1038/s42003-020-01259-8
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author Daisley, Brendan A.
Pitek, Andrew P.
Chmiel, John A.
Gibbons, Shaeley
Chernyshova, Anna M.
Al, Kait F.
Faragalla, Kyrillos M.
Burton, Jeremy P.
Thompson, Graham J.
Reid, Gregor
author_facet Daisley, Brendan A.
Pitek, Andrew P.
Chmiel, John A.
Gibbons, Shaeley
Chernyshova, Anna M.
Al, Kait F.
Faragalla, Kyrillos M.
Burton, Jeremy P.
Thompson, Graham J.
Reid, Gregor
author_sort Daisley, Brendan A.
collection PubMed
description Widespread antibiotic usage in apiculture contributes substantially to the global dissemination of antimicrobial resistance and has the potential to negatively influence bacterial symbionts of honey bees (Apis mellifera). Here, we show that routine antibiotic administration with oxytetracycline selectively increased tetB (efflux pump resistance gene) abundance in the gut microbiota of adult workers while concurrently depleting several key symbionts known to regulate immune function and nutrient metabolism such as Frischella perrera and Lactobacillus Firm-5 strains. These microbial changes were functionally characterized by decreased capped brood counts (marker of hive nutritional status and productivity) and reduced antimicrobial capacity of adult hemolymph (indicator of immune competence). Importantly, combination therapy with three immunostimulatory Lactobacillus strains could mitigate antibiotic-associated microbiota dysbiosis and immune deficits in adult workers, as well as maximize the intended benefit of oxytetracycline by suppressing larval pathogen loads to near-undetectable levels. We conclude that microbial-based therapeutics may offer a simple but effective solution to reduce honey bee disease burden, environmental xenobiotic exposure, and spread of antimicrobial resistance.
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spelling pubmed-75190522020-10-14 Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees Daisley, Brendan A. Pitek, Andrew P. Chmiel, John A. Gibbons, Shaeley Chernyshova, Anna M. Al, Kait F. Faragalla, Kyrillos M. Burton, Jeremy P. Thompson, Graham J. Reid, Gregor Commun Biol Article Widespread antibiotic usage in apiculture contributes substantially to the global dissemination of antimicrobial resistance and has the potential to negatively influence bacterial symbionts of honey bees (Apis mellifera). Here, we show that routine antibiotic administration with oxytetracycline selectively increased tetB (efflux pump resistance gene) abundance in the gut microbiota of adult workers while concurrently depleting several key symbionts known to regulate immune function and nutrient metabolism such as Frischella perrera and Lactobacillus Firm-5 strains. These microbial changes were functionally characterized by decreased capped brood counts (marker of hive nutritional status and productivity) and reduced antimicrobial capacity of adult hemolymph (indicator of immune competence). Importantly, combination therapy with three immunostimulatory Lactobacillus strains could mitigate antibiotic-associated microbiota dysbiosis and immune deficits in adult workers, as well as maximize the intended benefit of oxytetracycline by suppressing larval pathogen loads to near-undetectable levels. We conclude that microbial-based therapeutics may offer a simple but effective solution to reduce honey bee disease burden, environmental xenobiotic exposure, and spread of antimicrobial resistance. Nature Publishing Group UK 2020-09-25 /pmc/articles/PMC7519052/ /pubmed/32978472 http://dx.doi.org/10.1038/s42003-020-01259-8 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Daisley, Brendan A.
Pitek, Andrew P.
Chmiel, John A.
Gibbons, Shaeley
Chernyshova, Anna M.
Al, Kait F.
Faragalla, Kyrillos M.
Burton, Jeremy P.
Thompson, Graham J.
Reid, Gregor
Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
title Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
title_full Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
title_fullStr Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
title_full_unstemmed Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
title_short Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
title_sort lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7519052/
https://www.ncbi.nlm.nih.gov/pubmed/32978472
http://dx.doi.org/10.1038/s42003-020-01259-8
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