Circadian dynamics of the teleost skin immune-microbiome interface

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Abstract

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.

Related collections

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Author and article information

Contributors

Amy R. Ellison:

ORCID: http://orcid.org/0000-0003-3885-6077

a.ellison@bangor.ac.uk

Journal

Journal ID (nlm-ta): Microbiome

Journal ID (iso-abbrev): Microbiome

Title: Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2049-2618

Publication date (Electronic): 16 November 2021

Publication date PMC-release: 16 November 2021

Publication date Collection: 2021

Volume: 9

Electronic Location Identifier: 222

Affiliations

[1 ]GRID grid.7362.0, ISNI 0000000118820937, School of Natural Sciences, , Bangor University, ; Bangor, LL57 2DG UK

[2 ]GRID grid.8186.7, ISNI 0000000121682483, Institute of Biological, Environmental and Rural Sciences (IBERS), , Aberystwyth University, ; Aberystwyth, SY23 3DA UK

[3 ]GRID grid.5600.3, ISNI 0000 0001 0807 5670, School of Biosciences, , Cardiff University, ; Cardiff, CF10 3AX UK

Author information

Amy R. Ellison http://orcid.org/0000-0003-3885-6077

Article

Publisher ID: 1160

DOI: 10.1186/s40168-021-01160-4

PMC ID: 8594171

PubMed ID: 34782020

SO-VID: 02bb6b91-03bc-4327-a84c-a2f1c92f586a

License:

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/. The Creative Commons Public Domain Dedication waiver ( http://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.

History

Date received : 26 August 2021

Date accepted : 28 August 2021

Custom metadata

Keywords: circadian rhythm,clock gene expression,microbiome,parasite infection,fish,aquaculture,photoperiod,immunity,metagenome

Data availability:

Keywords: circadian rhythm, clock gene expression, microbiome, parasite infection, fish, aquaculture, photoperiod, immunity, metagenome