Abstract

Farmed fish are commonly exposed to stress in intensive aquaculture systems, often leading to immune impairment and increased susceptibility to disease. As microbial communities associated with the gut and skin are vital to host health and disease resilience, disruption of microbiome integrity could contribute to the adverse consequences of stress exposure. Little is known about how stress affects the fish microbiome, especially during sensitive early life stages when initial colonisation and proliferation of host-associated microbial communities take place. Therefore, we compared the effects of two aquaculture-relevant early-life stressors on the gut and skin microbiome of Atlantic salmon fry (four months post hatching) using 16S rRNA amplicon sequencing. Acute cold stress applied during late embryogenesis had a pronounced, lasting effect on the structure of the skin microbiome, as well as a less consistent effect on the gut microbiome. Follow-up targeted qPCR assays suggested that this is likely due to disruption of the egg shell microbial communities at the initial stages of microbiome colonisation, with persistent effects on community structure. In contrast, chronic post hatching stress altered the structure of the gut microbiome, but not that of the skin. Both types of stress promoted similar Gammaproteobacteria ASVs, particularly within the genera Acinetobacter and Aeromonas, which include several important opportunistic fish pathogens. Our results demonstrate the sensitivity of the salmon microbiome to environmental stressors during early life, with potential associated health impacts on the host. We also identified common signatures of stress in the salmon microbiome, which may represent useful microbial stress biomarkers.

Highlights

  • Aquaculture is the fastest growing food producing sector, and plays an increasingly important role in global food security in the face of a growing human population, depletion of capture fisheries and climate change (Teletchea and Fontaine, 2012)

  • We examined the effects of two contrasting, aquaculture-relevant stressors on the gut and skin micro­ biome of Atlantic salmon (Salmo salar): an acute stressor consisting of cold shock and air exposure during late embryogenesis, and chronic stress induced by lack of tank substrate/shelter for developing fry

  • As described in Uren Webster et al (2018), neither the acute cold shock or chronic post hatching stressor (475–1532 degree days (DD)) altered overall survival compared to the control group, and we observed no adverse effects on individual health

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Summary

Introduction

Aquaculture is the fastest growing food producing sector, and plays an increasingly important role in global food security in the face of a growing human population, depletion of capture fisheries and climate change (Teletchea and Fontaine, 2012). Increasing resistance to stress and disease is a priority in order to improve the sustainability of aquaculture. Disease and immune-related disorders is critically influenced by the host-associated microbiome (Rea et al, 2016). As for other vertebrates, microbial communities in the gut, skin and other mucosal surfaces have a fundamental influence on host health, including nutrient acquisition, metabolism, immune competence and disease resistance (de Bruijn et al, 2017; Koskella et al, 2017; Butt and Volkoff, 2019). Stress influences the brain-gutmicrobiota axis, including neural, immuno, and endocrine signalling pathways, via complex and interacting mechanisms (Foster et al, 2017). Disruption of the gut-brain axis, including microbiome dysbiosis, is linked to adverse health effects in mammals Disruption of the gut-brain axis, including microbiome dysbiosis, is linked to adverse health effects in mammals (e.g. Rea et al, 2016; Foster et al, 2017), and is likely to affect fish health and welfare too

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