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Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations

Microbiomes can enhance the health, fitness and even evolutionary potential of their hosts. Many organisms propagate favorable microbiomes fully or partially via vertical transmission. In the long term, such co-propagation can lead to the evolution of specialized microbiomes and functional interdepe...

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Autores principales: Kowallik, Vienna, Das, Ashutosh, Mikheyev, Alexander S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9751584/
https://www.ncbi.nlm.nih.gov/pubmed/36532456
http://dx.doi.org/10.3389/fmicb.2022.1030771
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author Kowallik, Vienna
Das, Ashutosh
Mikheyev, Alexander S.
author_facet Kowallik, Vienna
Das, Ashutosh
Mikheyev, Alexander S.
author_sort Kowallik, Vienna
collection PubMed
description Microbiomes can enhance the health, fitness and even evolutionary potential of their hosts. Many organisms propagate favorable microbiomes fully or partially via vertical transmission. In the long term, such co-propagation can lead to the evolution of specialized microbiomes and functional interdependencies with the host. However, microbiomes are vulnerable to environmental stressors, particularly anthropogenic disturbance such as antibiotics, resulting in dysbiosis. In cases where microbiome transmission occurs, a disrupted microbiome may then become a contagious pathology causing harm to the host across generations. We tested this hypothesis using the specialized socially transmitted gut microbiome of honey bees as a model system. By experimentally passaging tetracycline-treated microbiomes across worker ‘generations’ we found that an environmentally acquired dysbiotic phenotype is heritable. As expected, the antibiotic treatment disrupted the microbiome, eliminating several common and functionally important taxa and strains. When transmitted, the dysbiotic microbiome harmed the host in subsequent generations. Particularly, naïve bees receiving antibiotic-altered microbiomes died at higher rates when challenged with further antibiotic stress. Bees with inherited dysbiotic microbiomes showed alterations in gene expression linked to metabolism and immunity, among other pathways, suggesting effects on host physiology. These results indicate that there is a possibility that sublethal exposure to chemical stressors, such as antibiotics, may cause long-lasting changes to functional host-microbiome relationships, possibly weakening the host’s progeny in the face of future ecological challenges. Future studies under natural conditions would be important to examine the extent to which negative microbiome-mediated phenotypes could indeed be heritable and what role this may play in the ongoing loss of biodiversity.
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spelling pubmed-97515842022-12-16 Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations Kowallik, Vienna Das, Ashutosh Mikheyev, Alexander S. Front Microbiol Microbiology Microbiomes can enhance the health, fitness and even evolutionary potential of their hosts. Many organisms propagate favorable microbiomes fully or partially via vertical transmission. In the long term, such co-propagation can lead to the evolution of specialized microbiomes and functional interdependencies with the host. However, microbiomes are vulnerable to environmental stressors, particularly anthropogenic disturbance such as antibiotics, resulting in dysbiosis. In cases where microbiome transmission occurs, a disrupted microbiome may then become a contagious pathology causing harm to the host across generations. We tested this hypothesis using the specialized socially transmitted gut microbiome of honey bees as a model system. By experimentally passaging tetracycline-treated microbiomes across worker ‘generations’ we found that an environmentally acquired dysbiotic phenotype is heritable. As expected, the antibiotic treatment disrupted the microbiome, eliminating several common and functionally important taxa and strains. When transmitted, the dysbiotic microbiome harmed the host in subsequent generations. Particularly, naïve bees receiving antibiotic-altered microbiomes died at higher rates when challenged with further antibiotic stress. Bees with inherited dysbiotic microbiomes showed alterations in gene expression linked to metabolism and immunity, among other pathways, suggesting effects on host physiology. These results indicate that there is a possibility that sublethal exposure to chemical stressors, such as antibiotics, may cause long-lasting changes to functional host-microbiome relationships, possibly weakening the host’s progeny in the face of future ecological challenges. Future studies under natural conditions would be important to examine the extent to which negative microbiome-mediated phenotypes could indeed be heritable and what role this may play in the ongoing loss of biodiversity. Frontiers Media S.A. 2022-12-01 /pmc/articles/PMC9751584/ /pubmed/36532456 http://dx.doi.org/10.3389/fmicb.2022.1030771 Text en Copyright © 2022 Kowallik, Das and Mikheyev. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Kowallik, Vienna
Das, Ashutosh
Mikheyev, Alexander S.
Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
title Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
title_full Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
title_fullStr Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
title_full_unstemmed Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
title_short Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
title_sort experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9751584/
https://www.ncbi.nlm.nih.gov/pubmed/36532456
http://dx.doi.org/10.3389/fmicb.2022.1030771
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