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.

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

“…Though our study design did not allow us to assess causal relationships between microbiome variation and morbidity, we speculate that the microbiome shifts observed in fish that ultimately became moribund were related to corticosteroid-induced changes in immune function that led to increased susceptibility to opportunistic gill pathogens and ultimately to morbidity. In this regard, our findings align with previous studies in Atlantic salmon that identified associations between infectious disease and microbiome composition 19 , 30 , 64 , 65 . Bacterial gill disease, caused by a variety of opportunistic bacteria found in water, as well as infections by Aeromonas salmonicida and Ichthyobodo nector , are associated with fish that are immune compromised 66 – 68 .…”

Optimization of Low-Biomass Sample Collection and Quantitative PCR-Based Titration Impact 16S rRNA Microbiome Resolution

“…A common problem to both techniques is the high representation of host DNA relative to bacterial DNA, and this is further exacerbated by low-biomass samples, such as with mucous membranes. Birlanga et al ( 2 ) demonstrated this when they reported that salmon DNA represented three-quarters of the total returned reads when they analyzed salmon mucus in fish infected with AGD.…”

“…The gill microbiome also offers promise as a health management tool for high-value finfish aquaculture. Recent studies examining freshwater hatchery rearing ( 1 ), amoebic gill disease (AGD) ( 2 ), and the interplay of diet and rearing system ( 3 ) have all sought to exploit the aforementioned attributes. Intensive culture conditions in commercial aquaculture are fueling the development of noninvasive health management tools that seek to provide accuracy and protect fish welfare ( 4 ) with the potential to perform nonlethal longitudinal studies under commercial conditions.…”

“…The fish gill is the major respiratory organ and is surrounded by a mucus-rich layer that provides an extensive microbial niche. Recent gill microbiome studies have utilized terminal samples, such as gill fragments or entire gills ( 19 – 22 ), the gill filament without arch ( 23 ), or scraped gill mucus ( 2 , 24 ), with results showing the potential of the gill as an informative biological model. Swabs ( 1 , 25 ) offer an alternative noninvasive approach; however, data recovery must be shown to be robust, capturing the high spatial and temporal heterogenicity of real-world situations ( 2 , 26 ).…”

“…Recent gill microbiome studies have utilized terminal samples, such as gill fragments or entire gills ( 19 – 22 ), the gill filament without arch ( 23 ), or scraped gill mucus ( 2 , 24 ), with results showing the potential of the gill as an informative biological model. Swabs ( 1 , 25 ) offer an alternative noninvasive approach; however, data recovery must be shown to be robust, capturing the high spatial and temporal heterogenicity of real-world situations ( 2 , 26 ). Solubilization of membrane proteins and associated matrices using surfactants such as Tween and NP-40, which have differing levels of aggressiveness, is a commonly adopted approach in molecular biology to study extracellular surfaces.…”