Dataset Information

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. Video Abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s40168-021-01160-4.

SUBMITTER: Ellison A

PROVIDER: S-EPMC8594171 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe vertebrate clade diverged into Chondrichthyes (sharks, rays, and chimeras) and Osteichthyes fishes (bony fishes) approximately 420 mya, with each group accumulating vast anatomical and physiological differences, including skin properties. The skin of Chondrichthyes fishes is covered in dermal denticles, whereas Osteichthyes fishes are covered in scales and are mucous rich. The divergence time among these two fish groups is hypothesized to result in predictable variation among symbionts. Here, using shotgun metagenomics, we test if patterns of diversity in the skin surface microbiome across the two fish clades match predictions made by phylosymbiosis theory. We hypothesize (1) the skin microbiome will be host and clade-specific, (2) evolutionary difference in elasmobranch and teleost will correspond with a concomitant increase in host-microbiome dissimilarity, and (3) the skin structure of the two groups will affect the taxonomic and functional composition of the microbiomes.ResultsWe show that the taxonomic and functional composition of the microbiomes is host-specific. Teleost fish had lower average microbiome within clade similarity compared to among clade comparison, but their composition is not different among clade in a null based model. Elasmobranch's average similarity within clade was not different than across clade and not different in a null based model of comparison. In the comparison of host distance with microbiome distance, we found that the taxonomic composition of the microbiome was related to host distance for the elasmobranchs, but not the teleost fishes. In comparison, the gene function composition was not related to the host-organism distance for elasmobranchs but was negatively correlated with host distance for teleost fishes.ConclusionOur results show the patterns of phylosymbiosis are not consistent across both fish clades, with the elasmobranchs showing phylosymbiosis, while the teleost fish are not. The discrepancy may be linked to alternative processes underpinning microbiome assemblage, including possible historical host-microbiome evolution of the elasmobranchs and convergent evolution in the teleost which filter specific microbial groups. Our comparison of the microbiomes among fishes represents an investigation into the microbial relationships of the oldest divergence of extant vertebrate hosts and reveals that microbial relationships are not consistent across evolutionary timescales. Video abstract.

Project description:BackgroundHost-specific microbiomes play an important role in individual health and ecology; in marine mammals, epidermal microbiomes may be a protective barrier between the host and its aqueous environment. Understanding these epidermal-associated microbial communities, and their ecological- or health-driven variability, is the first step toward developing health indices for rapid assessment of individual or population health. In Cook Inlet, Alaska, an endangered population of beluga whales (Delphinapterus leucas) numbers fewer than 300 animals and continues to decline, despite more than a decade of conservation effort. Characterizing the epidermal microbiome of this species could provide insight into the ecology and health of this endangered population and allow the development of minimally invasive health indicators based on tissue samples.ResultsWe sequenced the hypervariable IV region of bacterial and archaeal SSU rRNA genes from epidermal tissue samples collected from endangered Cook Inlet beluga whales (n = 33) and the nearest neighboring population in Bristol Bay (n = 39) between 2012 and 2018. We examined the sequences using amplicon sequence variant (ASV)-based analyses, and no ASVs were associated with all individuals, indicating a greater degree of epidermal microbiome variability among beluga whales than in previously studied cetacean species and suggesting the absence of a species-specific core microbiome. Epidermal microbiome composition differed significantly between populations and across sampling years. Comparing the microbiomes of Bristol Bay individuals of known health status revealed 11 ASVs associated with potential pathogens that differed in abundance between healthy individuals and those with skin lesions or dermatitis. Molting and non-molting individuals also differed significantly in microbial diversity and the abundance of potential pathogen-associated ASVs, indicating the importance of molting in maintaining skin health.ConclusionsWe provide novel insights into the dynamics of Alaskan beluga whale epidermal microbial communities. A core epidermal microbiome was not identified across all animals. We characterize microbial dynamics related to population, sampling year and health state including level of skin molting. The results of this study provide a basis for future work to understand the role of the skin microbiome in beluga whale health and to develop health indices for management of the endangered Cook Inlet beluga whales, and cetaceans more broadly.