Comparative basal transcriptome profiles of the olfactory rosette and gills of Atlantic salmon (Salmo salar) unveil shared and distinct immunological features

The molecular repertoire of the mucosa-associated lymphoid tissue (MALT) in the olfactory rosette in most teleost fish is unknown. Here we present the basal transcriptome of the olfactory rosette of Atlantic salmon (Salmo salar). To investigate its mucosal immune features, we performed a comparative transcriptomic analysis with the gills, one of the most studied organs possessing MALT. Pathway enrichment revealed that cytokine-cytokine interaction and the neuroactive ligand-receptor interaction pathways were at the core of the shared similarity between the two organs. The immunological features of the two organs were further characterised by the overrepresentation of several immune-related pathways, particularly important for pathogen recognition. The immunological differences between the two organs were underlined with the differential regulation of markers for interleukins, extracellular matrix, antimicrobial peptides, and complement. The basal transcriptome of Atlantic salmon olfactory rosette is a valuable molecular toolbox that will advance our understanding of nasal immunity in teleost fish.publishedVersio

Editorial: Biology Meets Technology: Aquatic Animals in Novel and New Aquaculture Production Systems

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First report of Streptococcus parauberis in a cultured freshwater ornamental fish, the ram cichlid Mikrogeophagus ramirezi (Myers & Harry, 1948)

First paragraph: Since the first report of an outbreak of a streptococcal infection in rainbow trout (Oncorhynchus mykiss) in Japan in 1958 (Hoshina, Sano, & Morimoto,1958), streptococcosis has been responsible for significant mortalities resulting in considerable losses to the aquaculture industry (Noga,2010; Salati,2006). Numerous species from the family Streptococcaceae have been identified as aetiological agents of streptococcosis in fish (Noga,2010; Salati,2006; Toranzo, Magariños, & Romalde,2005), susceptibility to which was documented in both food (Inglis, Roberts, & Bromage,1993) and ornamental fish species (Russo, Mitchell, & Yanong,2006).Streptococcus parauberisis a coccoid, non-motile, alpha-haemolytic Gram-positive bacterium belonging to theStreptococcaceafamily (Nho etal.,2011) and has been reported as the aetiological agent of streptococcosis in a few fish species, including turbot (Scophthalmus maximus), olive flounder (Paralichthys olivaceus), sea bass (Sebastes ventricosus) and striped bass (Morone saxatilis) (Baeck, Kim, Gomez, & Park,2006; Domeénech etal.,1996; Haines etal.,2013; Mata etal.,2004; Oguro etal.,2014; Park etal.,2009).Streptococcus parauberishas been previously identified as the aetiological agent of bovine mastitis (Bradley,2002). It was formerly known asStreptococcustype II until comparative analysis of the sequence data ofStreptococcus uberistypes I and II showed that both were phylogenetically distinct, and the new speciesS.parauberiswas proposed (Williams and Collins1990)

Fast and slow releasing sulphide donors engender distinct transcriptomic alterations in Atlantic salmon hepatocytes

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Sulphide donors affect the expression of mucin and sulphide detoxification genes in the mucosal organs of Atlantic salmon (Salmo salar)

Hydrogen sulphide (H2S) is a gas that affects mucosal functions in mammals. However, its detrimental effects are less understood in fish despite being known to cause mass mortality. Here we used explant models to demonstrate the transcriptional responses of Atlantic salmon (Salmo salar) mucosa to the sulphide donor sodium hydrosulphide (NaHS). The study focused on two groups of genes: those encoding for sulphide detoxification and those for mucins. Moreover, we performed pharmacological studies by exposing the organ explants to mucus-interfering compounds and consequently exposed them to a sulphide donor. Exposure to NaHS significantly affected the expression of sulphide:quinone oxidoreductase (sqor1, sqor2) and mucin-encoding genes (muc5ac, muc5b). The general profile indicated that NaHS upregulated the expression of sulphide detoxification genes while a significant downregulation was observed with mucins. These expression profiles were seen in both organ explant models. Pharmacological stimulation and inhibition of mucus production used acetylcholine (ACh) and niflumic acid (NFA), respectively. This led to a significant regulation of the two groups of marker genes in the gills and olfactory rosette explants. Treatment of the mucosal organ explants with the mucus-interfering compounds showed that low dose NFA triggered more substantial changes while a dose-dependent response could not be established with ACh. Pharmacological interference demonstrated that mucins played a crucial role in mucosal protection against H2S toxicity. These results offer insights into how a sulphide donor interfered with mucosal responses of Atlantic salmon and are expected to contribute to our understanding of the least explored H2S-fish interactions—particularly at the mucosa.Sulphide donors affect the expression of mucin and sulphide detoxification genes in the mucosal organs of Atlantic salmon (Salmo salar)publishedVersio

Differential sensitivity of mucosal organs to transient exposure to hydrogen sulphide in post-smolt Atlantic salmon (Salmo salar)

Mortality related to hydrogen sulphide (H2S) has recently become a serious concern in Atlantic salmon (Salmo salar) farming, particularly in saline recirculating aquaculture systems (RASs), where the risk of H2S formation is high. H2S has a distinct odour of rotten eggs, and its production is associated with the anaerobic bacterial decomposition of protein and other sulphur-containing organic matter. Significant advances have been made in elucidating its formation in RAS, but the biological consequences of this toxicant in salmon remain elusive. We report the physiological consequences of transient exposure of post-smolt Atlantic salmon to H2S. The fish were exposed to one of three levels of H2S for 1 h: 0 µM (unexposed), 0.6 µM (low exposure), and 1.2 µM (high exposure). Fish were allowed to recover for 24 h and then sampled for gene expression, histology, and metabolomics analyses. Molecular profiling was performed on a subset of genes with known functions in sulphide detoxification, mucins, immunity, and stress responses, which focused on the gills, olfactory organ, skin, and distal gut. With the exception of interleukin 10, all genes studied were significantly affected in the skin, where high H2S triggered significant upregulation. Stress-related genes were mostly affected in the gills, where the high H2S level also induced significant upregulation. Downregulation of the marker genes was identified in the olfactory organ especially in the low-dose group. The distal gut was less sensitive to H2S, regardless of the dose. Histological health scoring of the four mucosal organs revealed no substantial structural alterations and only sporadic cases of mild-moderate unspecific tissue damage. High-throughput metabolomics revealed that transient H2S exposure had a substantial mucosal impact rather than a systemic impact, as shown by changes in skin mucus metabolome. Functional annotation indicated that 10 metabolomic pathways were significantly affected in the skin mucus, including tRNA charging, the superpathway of branched-chain amino acid biosynthesis, and glucosilinate biosynthesis from phenylalanine. The physiological alterations following transient exposure to H2S showed that the mucosal organs exhibited distinct response profiles, where transcriptional impacts were more pronounced in the skin and gills. The results contribute to a better understanding of the biological functions of exogenous H2S in teleost fish, as well as the development of mitigation strategies for salmon-production facilities and the risk of H2S exposure.Differential sensitivity of mucosal organs to transient exposure to hydrogen sulphide in post-smolt Atlantic salmon (Salmo salar)publishedVersio

The skin mucosal barrier of lumpfish (Cyclopterus lumpus L.) is weakened by exposure to potential aquaculture production related stressors

Various cleaner fish species, such as the lumpfish (Cyclopterus lumpus L.), are used in the sea cage production of Atlantic salmon (Salmo salar L.) as a control measure against the ectoparasitic salmon louse (Lepeophtheirus salmonis). However, during severe lice infestation, alternative treatments are required to control parasitic burden. The aim of this study was to gain insight into how lumpfish skin responds to different chemicals used to treat parasites. We collected skin from lumpfish from both research facilities (tank reared fish) and commercial production (cage reared fish), and used operational welfare indicators (OWIs), in vitro models, histology and transcriptomics to study how the skin responded to two anti-parasitic oxidative chemicals, hydrogen peroxide (H2O2) and peracetic acid (PAA). Lumpfish sampled from the farm were classified as clinically healthy or weak according to their morbidity status, and fish from each category were used to gain insight into how the therapeutics affect the skin barrier. Differences between healthy and weakened (moribund) fish, and between treated fish from each of the two groups, were observed. Histological examination showed an overall reduced skin quality in fish characterized as moribund, including different grades of exposed bony plates. In vitro oxidant-treated lumpfish skin had reduced migration capacity of keratocytes, a weakened epidermal barrier and altered gene transcription, changes that are known predisposing factors to secondary infections. Skin from non-treated, healthy fish sampled from commercial farms exhibited similar features and attributes to oxidant-exposed tank reared fish from a research facility, suggesting that apparently healthy cage-held lumpfish exhibited stress responses in the epidermal barrier. The results of the study outline the risks and consequences lumpfish can face if accidentally subjected to potential anti-parasitic oxidant treatments aimed at Atlantic salmon. It also strengthens the evidence behind the requirement that lumpfish should be removed from the cages before being potentially exposed to this type of treatment and outlines the potential risks of differing husbandry practices upon lumpfish health, welfare and resilience.The skin mucosal barrier of lumpfish (Cyclopterus lumpus L.) is weakened by exposure to potential aquaculture production related stressorspublishedVersio

Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts

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Multiomics Provide Insights into the Key Molecules and Pathways Involved in the Physiological Adaptation of Atlantic Salmon (Salmo salar) to Chemotherapeutic-Induced Oxidative Stress

Although chemotherapeutics are used to treat infections in farmed fish, knowledge on how they alter host physiology is limited. Here, we elucidated the physiological consequences of repeated exposure to the potent oxidative chemotherapeutic peracetic acid (PAA) in Atlantic salmon (Salmo salar) smolts. Fish were exposed to the oxidant for 15 (short exposure) or 30 (long exposure) minutes every 15 days over 45 days. Unexposed fish served as the control. Thereafter, the ability of the remaining fish to handle a secondary stressor was investigated. Periodic chemotherapeutic exposure did not affect production performance, though survival was lower in the PAA-treated groups than in the control. Increased ventilation, erratic swimming, and a loss of balance were common behavioural manifestations during the oxidant exposure. The plasma reactive oxygen species levels increased in the PAA-treated groups, particularly after the third exposure, suggesting an alteration in the systemic oxidative stress status. Plasma indicators for internal organ health were affected to a certain degree, with the changes mainly observed after the second and third exposures. Metabolomics disclosed that the oxidant altered several circulating metabolites. Inosine and guanosine were the two metabolites significantly affected by the oxidative stressor, regardless of exposure time. A microarray analysis revealed that the gills and liver were more responsive to the oxidant than the skin, with the gills being the most sensitive. Moreover, the magnitude of the transcriptomic modifications depended on the exposure duration. A functional analysis showed that genes involved in immunity and ribosomal functions were significantly affected in the gills. In contrast, genes crucial for the oxidation-reduction process were mainly targeted in the liver. Skin mucus proteomics uncovered that the changes in the mucosal proteome were dependent on exposure duration and that the oxidant interfered with ribosome-related processes. Mucosal mapping revealed gill mucous cell hypertrophy after the second and third exposures, although the skin morphological parameters remained unaltered. Lastly, repeated oxidant exposures did not impede the ability of the fish to mount a response to a secondary stressor. This study provides insights into how a chemical oxidative stressor alters salmon physiology at both the systemic and mucosal levels. This knowledge will be pivotal in developing an evidence-driven approach to the use of oxidative therapeutics in fish, with some of the molecules and pathways identified as potential biomarkers and targets for assessing the physiological cost of these treatments.publishedVersio

Nasal responses to elevated temperature and Francisella noatunensis infection in Atlantic cod (Gadus morhua)

We report the histological and transcriptomic changes in the olfactory organ of Atlantic cod exposed to Francisella noatunensis. Experimental infection was performed at either 12oC or 17oC. Infected fish presented the classic gross pathologies of francisellosis. Nasal morpho-phenotypic parameters were not significantly affected by temperature and infection, except for the number of mucus cells in the 12oC group seven weeks after the challenge. A higher number of genes were altered through time in the group reared at 17oC. At termination, the nasal transcriptome of infected fish in both groups was similar to the control. When both infected groups were compared, 754 DEGs were identified, many of which were involved in signalling, defence, transmembrane and enzymatic processes. In conclusion, the study reveals that elevated temperature could trigger responses in the olfactory organ of Atlantic cod and shape the nasal response to F. noatunensis infection.Nasal responses to elevated temperature and Francisella noatunensis infection in Atlantic cod (Gadus morhua)publishedVersio