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Circadian dynamics of the teleost skin immune-microbiome interface

BACKGROUND: Circadian rhythms of host immune activity and their microbiomes are likely pivotal to health and disease resistance. The integration of chronotherapeutic approaches to disease mitigation in managed animals, however, is yet to be realised. In aquaculture, light manipulation is commonly us...

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Autores principales: Ellison, Amy R., Wilcockson, David, Cable, Jo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8594171/
https://www.ncbi.nlm.nih.gov/pubmed/34782020
http://dx.doi.org/10.1186/s40168-021-01160-4
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author Ellison, Amy R.
Wilcockson, David
Cable, Jo
author_facet Ellison, Amy R.
Wilcockson, David
Cable, Jo
author_sort Ellison, Amy R.
collection PubMed
description BACKGROUND: Circadian rhythms of host immune activity and their microbiomes are likely pivotal to health and disease resistance. The integration of chronotherapeutic approaches to disease mitigation in managed animals, however, is yet to be realised. In aquaculture, light manipulation is commonly used to enhance growth and control reproduction but may have unknown negative consequences for animal health. Infectious diseases are a major barrier to sustainable aquaculture and understanding the circadian dynamics of fish immunity and crosstalk with the microbiome is urgently needed. RESULTS: Here, using rainbow trout (Oncorhynchus mykiss) as a model, we combine 16S rRNA metabarcoding, metagenomic sequencing and direct mRNA quantification methods to simultaneously characterise the circadian dynamics of skin clock and immune gene expression, and daily changes of skin microbiota. We demonstrate daily rhythms in fish skin immune expression and microbiomes, which are modulated by photoperiod and parasitic lice infection. We identify putative associations of host clock and immune gene profiles with microbial composition. Our results suggest circadian perturbation, that shifts the magnitude and timing of immune and microbiota activity, is detrimental to fish health. CONCLUSIONS: The substantial circadian dynamics and fish host expression-microbiome relationships we find represent a valuable foundation for investigating the utility of chronotherapies in aquaculture, and more broadly contributes to our understanding of the role of microbiomes in circadian health of vertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01160-4.
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spelling pubmed-85941712021-11-16 Circadian dynamics of the teleost skin immune-microbiome interface Ellison, Amy R. Wilcockson, David Cable, Jo Microbiome Research BACKGROUND: Circadian rhythms of host immune activity and their microbiomes are likely pivotal to health and disease resistance. The integration of chronotherapeutic approaches to disease mitigation in managed animals, however, is yet to be realised. In aquaculture, light manipulation is commonly used to enhance growth and control reproduction but may have unknown negative consequences for animal health. Infectious diseases are a major barrier to sustainable aquaculture and understanding the circadian dynamics of fish immunity and crosstalk with the microbiome is urgently needed. RESULTS: Here, using rainbow trout (Oncorhynchus mykiss) as a model, we combine 16S rRNA metabarcoding, metagenomic sequencing and direct mRNA quantification methods to simultaneously characterise the circadian dynamics of skin clock and immune gene expression, and daily changes of skin microbiota. We demonstrate daily rhythms in fish skin immune expression and microbiomes, which are modulated by photoperiod and parasitic lice infection. We identify putative associations of host clock and immune gene profiles with microbial composition. Our results suggest circadian perturbation, that shifts the magnitude and timing of immune and microbiota activity, is detrimental to fish health. CONCLUSIONS: The substantial circadian dynamics and fish host expression-microbiome relationships we find represent a valuable foundation for investigating the utility of chronotherapies in aquaculture, and more broadly contributes to our understanding of the role of microbiomes in circadian health of vertebrates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01160-4. BioMed Central 2021-11-16 /pmc/articles/PMC8594171/ /pubmed/34782020 http://dx.doi.org/10.1186/s40168-021-01160-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ellison, Amy R.
Wilcockson, David
Cable, Jo
Circadian dynamics of the teleost skin immune-microbiome interface
title Circadian dynamics of the teleost skin immune-microbiome interface
title_full Circadian dynamics of the teleost skin immune-microbiome interface
title_fullStr Circadian dynamics of the teleost skin immune-microbiome interface
title_full_unstemmed Circadian dynamics of the teleost skin immune-microbiome interface
title_short Circadian dynamics of the teleost skin immune-microbiome interface
title_sort circadian dynamics of the teleost skin immune-microbiome interface
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8594171/
https://www.ncbi.nlm.nih.gov/pubmed/34782020
http://dx.doi.org/10.1186/s40168-021-01160-4
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