Dataset Information

Dynamic gill and mucus microbiomes during a gill disease episode in farmed Atlantic salmon.

ABSTRACT: Amoebic gill disease (AGD) and complex gill disease (CGD) are recurrent gill disorders in Atlantic salmon, resulting in significant aquaculture losses. The role of gill microbiomes in gill disease development is unclear. We undertook a longitudinal study to characterise the gill tissue and gill mucus microbiomes of farmed Atlantic salmon before, and during, a gill disease episode. Using a newly optimised DNA extraction protocol, we sequenced rRNA genes from microbiomes of gill samples taken from 105 individual salmon on a farm, over a summer season. The AGD aetiological agent, Neoparamoeba perurans, was PCR-quantified targeting 18S rRNA genes. Similar analyses were carried out on mucus samples. Mucus scrapings were suitable, non-lethal substitutes for characterisation of the gill prokaryotic community in this study. Gill tissue and gill mucus microbiomes changed during the campaign, correlating with N. perurans concentrations. Time explained 35% of the gill tissue and gill mucus microbiome variance, while N. perurans concentrations explained 5%. Genera including Dyadobacter, Shewanella and Pedobacter were maximally abundant in gill and mucus samples at the timepoint prior to the the detection of gill disorder signs, at T3. Shewanella was significantly more abundant before than during the gill disease episode, and we suggest this genus could be considered in future studies addressing relationships between gill disease and the gill microbiome.

SUBMITTER: Birlanga VB

PROVIDER: S-EPMC9537138 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Dynamic gill and mucus microbiomes during a gill disease episode in farmed Atlantic salmon.

Birlanga Victor B VB McCormack Grace G Ijaz Umer Z UZ MacCarthy Eugene E Smith Cindy C Collins Gavin G

Scientific reports 20221006 1

Amoebic gill disease (AGD) and complex gill disease (CGD) are recurrent gill disorders in Atlantic salmon, resulting in significant aquaculture losses. The role of gill microbiomes in gill disease development is unclear. We undertook a longitudinal study to characterise the gill tissue and gill mucus microbiomes of farmed Atlantic salmon before, and during, a gill disease episode. Using a newly optimised DNA extraction protocol, we sequenced rRNA genes from microbiomes of gill samples taken from ...[more]

PMID: 36202859

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Project description:Various agents including Ca. Piscichlamydia salmonis, Ca. Branchiomonas cysticola, Desmozoon lepeophtherii, Paramoeba perurans and salmon gill poxvirus may be associated with complex gill disease in Atlantic salmon. Co-infections involving two or more of these agents are common and histopathological interpretation of lesions is therefore challenging. In this study, we developed a semi-quantitative scoring system for examination of histopathological gill lesions in sea-farmed Atlantic salmon suffering from gill disease. Following qPCR analysis of gills sampled for Ca. P. salmonis, Ca. B. cysticola, D. lepeophtherii and P. perurans from 22 geographically spread outbreaks, five cases representing different infectious loads and combinations of agents were chosen for histopathological scoring. Twenty-eight histological features were evaluated and potential associations between individual pathological changes and the occurrence of individual agents studied. The inter-observer agreement in interpretation of histological parameters between the three pathologists involved, was calculated to validate robustness of the scoring scheme. Seventeen histological parameters met the criteria for inter-observer agreement analysis and were included in the calculation. The three most frequent findings were identification of subepithelial leukocytes, epithelial cell hyperplasia and mucus cell hyperplasia. While few findings could be specifically related to particular agents, necrosis in hyperplastic lesions, pustules and necrosis of subepithelial cells appeared to be associated with the presence of Ca. B. cysticola. Further, lesion profiles clearly support the previously identified association between P. perurans and pathological changes associated with AGD. Very few pathological changes were observed in the single case in which Ca. P. salmonis was the dominating agent. Some lesions were only very rarely observed e.g. chloride cell necrosis, epithelial cell apoptosis, lamellar deposition of melanin and haemophagocytosis. The scoring scheme developed and applied was robust and sensitive. A less extensive scheme for routine diagnostic use is proposed.

Project description:Understanding the relationship between resident microbiota and disease in cultured fish represents an important and emerging area of study. Marine gill disorders in particular are considered an important challenge to Atlantic salmon (Salmo salar) aquaculture, however relatively little is known regarding the role resident gill microbiota might play in providing protection from or potentiating different gill diseases. Here, 16S rRNA sequencing was used to examine the gill microbiome alongside fish health screening in farmed Atlantic salmon. Results were used to explore the relationship between microbial communities and gill disease. Microbial community restructuring was observed throughout the sampling period and linked to varied drivers of change, including environmental conditions and severity of gill pathology. Taxa with significantly greater relative abundance on healthier gills included isolates within genus Shewanella, and taxa within family Procabacteriaceae. In contrast, altered abundance of Candidatus Branchiomonas and Rubritalea spp. were associated with damaged gills. Interestingly, more general changes in community richness and diversity were not associated with altered gill health, and thus not apparently deleterious to fish. Gross and histological gill scoring demonstrated seasonal shifts in gill pathology, with increased severity of gill damage in autumn. Specific infectious causes that contributed to observed pathology within the population included the gill disorder amoebic gill disease (AGD), however due to the uncontrolled nature of this study and likely mixed contribution of various causes of gill disease to observed pathology results do not strongly support an association between the microbial community and specific infectious or non-infectious drivers of gill pathology. Results suggest that the microbial community of farmed Atlantic salmon gills undergo continual restructuring in the marine environment, with mixed influences upon this change including environmental, host, and pathogenic factors. A significant association of specific taxa with different gill health states suggests these taxa might make meaningful indicators of gill health. Further research with more frequent sampling and deliberate manipulation of gills would provide important advancement of knowledge in this area. Overall, although much is still to be learnt regarding what constitutes a healthy or maladapted gill microbial community, the results of this study provide clear advancement of the field, providing new insight into the microbial community structure of gills during an annual production cycle of marine-stage farmed Atlantic salmon.

Project description:BackgroundSalmon aquaculture involves freshwater and seawater phases. Recently there has been an increase in multifactorial gill health challenges during the seawater phase which has led to an urgent need to understand the gill microbiome. There is a lack of understanding on what drives the composition of the gill microbiome, and the influence the freshwater stage has on its long-term composition. We characterise the gill microbiome from seven cohorts of Atlantic salmon raised in six different freshwater operational systems-recirculating aquaculture system (RAS), flowthrough (FT) and loch-based system, prior to and after transfer to seven seawater farms, over two different input seasons, S0 (2018) and S1 (2019).ResultsUsing the V1-V2 region of the 16S rRNA gene, we produced amplicon libraries absent of host contamination. We showed that hatchery system influenced the gill microbiome (PERMAOVA R2 = 0.226, p < 0.001). Loch and FT systems were more similar to each other than the three RAS systems, which clustered together. On transfer to sea, the gill microbiomes of all fish changed and became more similar irrespective of the initial hatchery system, seawater farm location or season of input. Even though the gill microbiome among seawater farm locations were different between locations (PERMAOVA R2 = 0.528, p < 0.001), a clustering of the gill microbiomes by hatchery system of origin was still observed 7-25 days after transfer (PERMAOVA R = 0.164, p < 0.001). Core microbiomes at genera level were observed among all fish in addition to freshwater only, and seawater only. At ASV level core microbiomes were observed among FT and loch freshwater systems only and among all seawater salmon. The gill microbiome and surrounding water at each hatchery had more shared ASVs than seawater farms.ConclusionWe showed hatchery system, loch, FT or RAS, significantly impacted the gill microbiome. On transfer to sea, the microbiomes changed and became more similar. After transfer, the individual sites to which the fish were transferred has a significant influence on microbiome composition, but interesting some clustering by hatchery system remained. Future gill disease mitigation methods that target enhancing the gill microbiome may be most effective in the freshwater stage, as there were more shared ASVs between water and gill at hatchery, compared to at sea.

Dataset Information

Dynamic gill and mucus microbiomes during a gill disease episode in farmed Atlantic salmon.

Publications

Dynamic gill and mucus microbiomes during a gill disease episode in farmed Atlantic salmon.

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