Circadian dynamics of the teleost skin immune-microbiome interface

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.

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“…Compared with the traditional tools for rhythmicity detection, such as JTK_Cycle, Bio_Cycle, and RAIN, CircaCompare provides a means to quantify and statistically support differences between rhythms, specific to the characteristic desired (MESOR, amplitude, and phase) with high sensitivity ( 33 ). To the best of our knowledge, it is the latest tool for comparison between rhythms directly ( 60 , 61 ). We took advantage of this tool to explore the circadian characteristics in the gestational mice.…”

Exploring the alterations and function of skin microbiome mediated by ionizing radiation injury

“…Skin sample preparation and 16S ribosomal RNA (rRNA) sequencing were conducted as previously described ( Ellison et al., 2021 ; Olesen et al., 2022 ). Genomic DNA was extracted using Wizard ® Genomic DNA Purification Kit (Promega, Madison, WI, USA) according to the manufacturer’s protocol.…”

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