Abstract

BackgroundCircadian 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.ResultsHere, 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.ConclusionsThe 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.85h9CE3kvpyMkhkCbi-Bj-Video

Highlights

  • Circadian rhythms—endogenous daily cycles in physiological and behavioural processes—are a ubiquitous phenomenon to life

  • Using rainbow trout (Oncorhynchus mykiss) as a model, we combine 16S rRNA gene metabarcoding and direct mRNA quantification methods to simultaneously characterise the circadian dynamics of skin clock and immune gene expression, and daily changes of skin microbiota

  • Infected rainbow trout had significantly higher expression of 24 immune genes (89%) under 12:12 LD, whereas only 14 (52%) were significantly higher in infected fish compared to healthy controls under constant light (Fig. 1)

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Summary

Introduction

Circadian rhythms—endogenous daily cycles in physiological and behavioural processes—are a ubiquitous phenomenon to life. Circadian rhythms are orchestrated by ‘clock genes’ driving transcriptional-translational autoregulatory feedback loops [1], which are transduced to temporally coordinate biological activities. A primary function of immune systems is to protect the host from invading pathogenic microbes. Animals are invariably colonised by a suite of microorganisms—their ‘microbiome’—which span the spectrum of symbiosis from mutualists to opportunistic pathogens. 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, is yet to be realised. 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

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