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Cortisol-Related Signatures of Stress in the Fish Microbiome.

ABSTRACT: Exposure to environmental stressors can compromise fish health and fitness. Little is known about how stress-induced microbiome disruption may contribute to these adverse health effects, including how cortisol influences fish microbial communities. We exposed juvenile Atlantic salmon to a mild confinement stressor for two weeks. We then measured cortisol in the plasma, skin-mucus, and feces, and characterized the skin and fecal microbiome. Fecal and skin cortisol concentrations increased in fish exposed to confinement stress, and were positively correlated with plasma cortisol. Elevated fecal cortisol was associated with pronounced changes in the diversity and structure of the fecal microbiome. In particular, we identified a marked decline in the lactic acid bacteria Carnobacterium sp. and an increase in the abundance of operational taxonomic units within the classes Clostridia and Gammaproteobacteria. In contrast, cortisol concentrations in skin-mucus were lower than in the feces, and were not related to any detectable changes in the skin microbiome. Our results demonstrate that stressor-induced cortisol production is associated with disruption of the gut microbiome, which may, in turn, contribute to the adverse effects of stress on fish health. They also highlight the value of using non-invasive fecal samples to monitor stress, including simultaneous determination of cortisol and stress-responsive bacteria.

SUBMITTER: Uren Webster TM

PROVIDER: S-EPMC7381252 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Cortisol-Related Signatures of Stress in the Fish Microbiome.

Uren Webster Tamsyn M TM Rodriguez-Barreto Deiene D Consuegra Sofia S Garcia de Leaniz Carlos C

Frontiers in microbiology 20200714

Exposure to environmental stressors can compromise fish health and fitness. Little is known about how stress-induced microbiome disruption may contribute to these adverse health effects, including how cortisol influences fish microbial communities. We exposed juvenile Atlantic salmon to a mild confinement stressor for two weeks. We then measured cortisol in the plasma, skin-mucus, and feces, and characterized the skin and fecal microbiome. Fecal and skin cortisol concentrations increased in fish ...[more]

PMID: 32765459

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Project description:BackgroundAquaculture is a fast-growing industry and therefore welfare and environmental impact have become of utmost importance. Preventing stress associated to common aquaculture practices and optimizing the fish stress response by quantification of the stress level, are important steps towards the improvement of welfare standards. Stress is characterized by a cascade of physiological responses that, in-turn, induce further changes at the whole-animal level. These can either increase fitness or impair welfare. Nevertheless, monitorization of this dynamic process has, up until now, relied on indicators that are only a snapshot of the stress level experienced. Promising technological tools, such as proteomics, allow an unbiased approach for the discovery of potential biomarkers for stress monitoring. Within this scope, using Gilthead seabream (Sparus aurata) as a model, three chronic stress conditions, namely overcrowding, handling and hypoxia, were employed to evaluate the potential of the fish protein-based adaptations as reliable signatures of chronic stress, in contrast with the commonly used hormonal and metabolic indicators.ResultsA broad spectrum of biological variation regarding cortisol and glucose levels was observed, the values of which rose higher in net-handled fish. In this sense, a potential pattern of stressor-specificity was clear, as the level of response varied markedly between a persistent (crowding) and a repetitive stressor (handling). Gel-based proteomics analysis of the plasma proteome also revealed that net-handled fish had the highest number of differential proteins, compared to the other trials. Mass spectrometric analysis, followed by gene ontology enrichment and protein-protein interaction analyses, characterized those as humoral components of the innate immune system and key elements of the response to stimulus.ConclusionsOverall, this study represents the first screening of more reliable signatures of physiological adaptation to chronic stress in fish, allowing the future development of novel biomarker models to monitor fish welfare.

Project description:BackgroundImmunoglobulin G4-related disease (IgG4-RD) and systemic sclerosis (SSc) are rare autoimmune diseases characterized by the presence of CD4+ cytotoxic T cells in the blood as well as inflammation and fibrosis in various organs, but they have no established etiologies. Similar to other autoimmune diseases, the gut microbiome might encode disease-triggering or disease-sustaining factors.MethodsThe gut microbiomes from IgG4-RD and SSc patients as well as healthy individuals with no recent antibiotic treatment were studied by metagenomic sequencing of stool DNA. De novo assembly-based taxonomic and functional characterization, followed by association and accessory gene set enrichment analysis, were applied to describe microbiome changes associated with both diseases.ResultsMicrobiomes of IgG4-RD and SSc patients distinctly separated from those of healthy controls: numerous opportunistic pathogenic Clostridium and typically oral Streptococcus species were significantly overabundant, while Alistipes, Bacteroides, and butyrate-producing species were depleted in the two diseases compared to healthy controls. Accessory gene content analysis in these species revealed an enrichment of Th17-activating Eggerthella lenta strains in IgG4-RD and SSc and a preferential colonization of a homocysteine-producing strain of Clostridium bolteae in SSc. Overabundance of the classical mevalonate pathway, hydroxyproline dehydratase, and fibronectin-binding protein in disease microbiomes reflects potential functional differences in host immune recognition and extracellular matrix utilization associated with fibrosis. Strikingly, the majority of species that were differentially abundant in IgG4-RD and SSc compared to controls showed the same directionality in both diseases. Compared with multiple sclerosis and rheumatoid arthritis, the gut microbiomes of IgG4-RD and SSc showed similar signatures; in contrast, the most differentially abundant taxa were not the facultative anaerobes consistently identified in inflammatory bowel diseases, suggesting the microbial signatures of IgG4-RD and SSc do not result from mucosal inflammation and decreased anaerobism.ConclusionsThese results provide an initial characterization of gut microbiome ecology in fibrosis-prone IgG4-RD and SSc and reveal microbial functions that offer insights into the pathophysiology of these rare diseases.

Dataset Information

Cortisol-Related Signatures of Stress in the Fish Microbiome.

Publications

Cortisol-Related Signatures of Stress in the Fish Microbiome.

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