Early life stress causes persistent impacts on the microbiome of Atlantic salmon

Webster, Tamsyn M. Uren

doi:10.1101/2020.01.16.908939

Cited by 6 publications

(9 citation statements)

References 55 publications

(86 reference statements)

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“…Our finding that corticosteroid treatments affect gut microbiome diversity and composition is consistent with studies in other organisms. Previous studies showed that cortisol elevation due to acute stressors associates with altered diversity and composition of the gut and skin microbiome in Atlantic salmon (Salmo salar) 16,18 . Specific environmental stressors, including thermal stress 55,56 and crowding stress 57 modulate the microbiota of other fish species.…”

Section: Discussionmentioning

confidence: 99%

Gut microbiome composition associates with corticosteroid treatment, morbidity, and senescence in Chinook salmon (Oncorhynchus tshawytscha)

Couch

Neal

Herron

et al. 2023

Sci Rep

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Pacific salmon experience prolonged elevation in corticosteroid hormones during important life history events including migration, reproduction, and senescence. These periods of elevated corticosteroids correspond with changes to immunity and energy metabolism; therefore, fish may be particularly vulnerable to mortality at these times. Recent studies found that stress-induced cortisol release associated with microbial community shifts in salmonids, raising the question of how longer-term corticosteroid dynamics that accompany life history transitions affect salmonid microbiomes. In this work, we experimentally evaluated the relationships between gut microbiome composition, chronically elevated corticosteroids, and mortality in juvenile Chinook salmon (Oncorhynchus tshawytscha). We found that treatment with slow-release implants of the corticosteroids cortisol or dexamethasone resulted in changes to the gut microbiome. Morbidity was also associated with microbiome composition, suggesting that the gut microbiome reflects individual differences in susceptibility to opportunistic pathogens. Additionally, we analyzed a small number of samples from adult fish at various stages of senescence. Results from these samples suggest that microbiome composition associated with gut integrity, and that the microbial communities of corticosteroid treated juveniles shift in composition toward those of senescent adults. Overall, findings from this work indicate that the gut microbiome correlates with mortality risk during periods of chronic corticosteroid elevation.

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Section: Discussionmentioning

confidence: 99%

Gut microbiome composition associates with corticosteroid treatment, morbidity, and senescence in Chinook salmon (Oncorhynchus tshawytscha)

Couch

Neal

Herron

et al. 2023

Sci Rep

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“…Existing research on the gut microbiome of freshwater Atlantic salmon suggests that even when alpha diversity is not altered, difference may be present in the beta diversity, for example, Chao1 richness and Shannon diversity were not altered by acute cold stress or a chronic environmental stress but the beta diversity was altered 57 . In early stage salmonids when the dietary protein composition is altered, existing studies observed a signi cant shift in the beta diversity and composition of the gut microbiome, in Atlantic salmon (Salmo salar) 58 , in Rainbow trout (Oncorhynchus mykiss) 35,59 , and in Arctic charr (Salvelinus alpinus) 60 .…”

Section: Discussionmentioning

confidence: 99%

Torula Yeast in the Diet of Atlantic Salmon Salmo Salar and the Impact on Growth Performance and Gut Microbiome.

Leeper

Ekmay

Knobloch

et al. 2021

Preprint

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Atlantic salmon aquaculture is expanding, and with it, the need to find suitable replacements for conventional protein sources used in formulated feeds. Torula yeast (Cyberlindnera jadinii), has been identified as a promising alternative protein for feeds and can be sustainably cultivated from lignocellulosic biomasses. The present study investigates the impact of torula yeast on the growth performance and the gut microbiome of freshwater Atlantic salmon. Both a marine protein base diet and a mixed marine and plant protein base diet were tested, where conventional proteins were replaced with increasing inclusion levels of torula yeast, (0%, 10%, 20%). This study demonstrated that 20% torula yeast can replace fish meal without alteration to growth performance while leading to potential benefits for the gut microbiome by increasing the presence of bacteria positively associated with the host. However, when torula yeast replaced plant meal in a mixed protein diet, results suggest 10% inclusion of yeast produced the best growth performance results and at the highest inclusion level, potentially negative changes were observed in the gut microbial community, such as a decrease in lactic acid bacteria. This study supports the continued investigation of torula yeast for Atlantic salmon as a partial replacement for conventional proteins.

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“…and Aeromonas sp, were also particularly abundant in fish that had high levels of faecal cortisol. These genera include a range of opportunistic fish pathogens (Austin & Austin 2007), and tend to increase following exposure to different types of environmental stress in fish (Boutin et al 2013; Uren Webster et al 2019), suggesting they may represent a common signature of stress exposure. In mammals, experimental administration of cortisol results in a similar reduction in probiotic lactic acid-producing bacteria and an increase in pro-inflammatory microbiota (Huang et al 2015; Petrosus et al 2018; Wu et al 2018), suggesting that these bacteria taxa could represent useful biomarkers of stress across vertebrates.…”

Section: Discussionmentioning

confidence: 99%

“…Disruption of the microbiome is likely to represent an important mechanism by which stress affects fish health, welfare and performance in aquaculture. There is some evidence that environmental and social stressors disrupt microbial communities associated with the fish gut and skin (Boutin et al 2013; Sylvain et al 2016; Uren Webster et al 2019; Zha et al 2018), however, a potential role of cortisol in mediating these effects is unknown. We hypothesised that stress-induced cortisol production would directly disrupt the fish microbiome.…”

Section: Introductionmentioning

confidence: 99%

Cortisol-induced signatures of stress in the fish microbiome

Webster

Rodríguez‐Barreto

Consuegra

et al. 2019

Preprint

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Stress experienced in intensive aquaculture can compromise fish growth, condition and immunity. Microbiome disruption may contribute to these adverse health effects, but little is known about how stress affects fish microbial communities. Here, we specifically examined the effects of stress-induced cortisol production on the fish microbiome. We exposed juvenile Atlantic salmon to a mild confinement stressor for two weeks. We then measured cortisol in the plasma, skin-mucus and faeces, and characterised the skin and faecal microbiome. Faecal and skin cortisol concentrations increased in fish exposed to confinement stress, and were positively correlated with plasma cortisol. Elevated faecal cortisol was associated with pronounced changes in the diversity and structure of the faecal microbiome. In particular, we identified a marked decline in probiotic Lactobacillales (Carnobacterium sp.) and an increase in pro-inflammatory and pathogenic taxa within the classes Clostridia and Gammaproteobacteria. In contrast, skin-mucus cortisol concentrations were lower and not associated with any detectable changes in the skin microbiome. Our results demonstrate that cortisol disrupts 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 faecal samples to monitor stress, including simultaneous determination of cortisol and stress-responsive bacteria.

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Early life stress causes persistent impacts on the microbiome of Atlantic salmon

Abstract: 1

Cited by 6 publications

References 55 publications

Gut microbiome composition associates with corticosteroid treatment, morbidity, and senescence in Chinook salmon (Oncorhynchus tshawytscha)

Gut microbiome composition associates with corticosteroid treatment, morbidity, and senescence in Chinook salmon (Oncorhynchus tshawytscha)

Torula Yeast in the Diet of Atlantic Salmon Salmo Salar and the Impact on Growth Performance and Gut Microbiome.

Cortisol-induced signatures of stress in the fish microbiome

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