Effect of chronic exposure to ammonia on alterations of proteins and immunoglobulins in sea bass (Dicentrarchus labrax) serum
Introduction
Under intensive rearing conditions, and particularly when the water is recycled, the ammonia concentration in the water may increase. The ammonia in the water is the sum of two forms, the unionized fraction NH3 and the ionized fraction NH4+. The relative proportion of the two forms depends on pH, temperature and salinity. The former is much more toxic than the latter but toxicity is probably due to a contribution of both forms [8]. The convention is to express ammonia concentration in terms of total ammonia nitrogen (TA-N) and unionized ammonia nitrogen (UIA-N). The specific biochemical mechanism of ammonia toxicity in fish is not fully explained, but it has been shown that ammonia intoxication impairs ATP production, induces a store depletion of polysaccharide and plasma ions, alters the neuronal synaptic transmission, induces leucopenia, erythropenia, inflammation and degeneration of gills and kidneys [8].
The ammonia 96-h LC50 (lethal concentration for 50 % of a population exposed for 96 h to ammonia) ranges from 0.32 mg.L-1UIA-N in rainbow trout (Oncorhynchus mykiss) to 3.1 mg.L-1UIA-N in channel catfish (Ictalarus punctatus) [8]. The 96-h LC50 for striped bass (Morone saxatilis) is 1.01 mg.L-1UIA-N and 0.64 mg.L-1UIA-N for another freshwater dicentrarchid, the hybrid striped bass (M. saxatilis × M. chrysops) [11].
Although data in sea water are still scarce, the 96-h LC50 is 1.70 mg.L-1UIA-N for the sea bass juveniles (Dicentrarchus labrax), 2.55 mg.L-1UIA-N for the both sea bream (Sparus aurata) and turbot (Psetta maxima) [13] and 0.45 mg.L-1UIA-N for fingerling coho salmon (Oncorhynchus kisutch) [3].
An ammonia molecule is too small to act as an antigen and cannot directly modify the immune system by acting in the usual way. Moreover, it is a natural endogenous product of fish. However, during acute ammonia poisoning in fingerling coho salmon, high ammonia would be considered to act indirectly on the immune system through its toxic action or as a stressor [10].
The immune response can be modified by several stessors. Both defence mechanisms and non-specific activity may be affected [1]. However, sometimes polluant stressors may enhance certain defence parameters, e.g. an increase in circulating antibodies in the serum of striped bass exposed to water with small amounts of cadmium [15]. More recently, it has been found that antibody concentrations, after vaccination of rainbow trout against Streptococcus iniae, are higher in fish exposed to ammonia; however, there was no correlation with protection [6].
The aim of this study was to examine the correlation between chronic ammonia exposure and alteration in Ig, and total protein concentrations or in the protein molecular weight profile (PMWP), as well as evaluating, by a non-lethal procedure, the capability of sea bass to compensate for these alterations.
Section snippets
Fish
For the duration of the experiment, the fish were reared in a soundproofed room with controlled light and environmental parameters. Each tank (1 m3) received a flow of 1 m3.h-1of sea water, which was filtered (20 mm) and UV sterilized and contained the selected ammonia concentration. Temperature was kept at 22 ± 1 °C, inlet O2 was maintained between 120 and 150 % and outlet over 80 % of saturation [8].
The sea bass were provided by our Ifremer laboratory holding facilities. They were fed on a
Duplicate
Each group was followed in duplicate and non-statistical differences were found between duplicates for protein or Ig concentrations (0.94 < P < 0.09 with 28 degrees of freedom). Consequently, data from the duplicate groups were pooled and treated as one group for further analysis.
Serum concentration (table I)
On day 21 of the exposure period the protein concentrations ( figure 1, lines) of the treated groups were significantly lower than the control group concentration (group 0: 40.74 ± 1.70 mg.mL-1; group 1: 37.24 ± 1.84
Discussion
First of all, a variation in protein and Ig concentrations versus time of the control group was observed. Protein concentration alterations over the year have been recorded in sea bass broodstock [5]. A regular increase has also been observed in protein and Ig serum concentrations in sea bass fry from 40 up to 200 g in weight, with fluctuation before stabilization around 350 g in weight.
Actually, most agents investigated as stress have other detrimental actions (infection, toxicity, etc.) [1].
Acknowledgements
We are grateful to Dr Stuart Hetherington of Mannin Seafarm, Isle of Man for critical reading of the manuscript.
References (20)
- et al.
Isolation and partial characterization of IgM-like seabass (Dicentrarchus labrax L., 1758) immunoglobulins
Aquaculture
(1995) - et al.
Ontogeny of IgM-bearing cells and changes in the immunoglobulin M-like protein level (IgM) during larval stages in sea bass (Dicentrarchus labrax)
Fish Shellfish Immunol.
(1997) - et al.
Alterations in total protein IgM and specific antibody activity of male and female sea bass (Dicentrarchus labrax L., 1758) serum following injection with killed Vibrio anguillarum
Fish Shellfish Immunol.
(1997) - et al.
Effect of ammonia on the survival and the immune response of rainbow trout (Oncorhynchus mikiss Walbaum) vaccined against Streptococcus iniae,
Fish Shellfish Immunol.
(1997) Paradoxical effects of cadmium exposure an antibacterial antibody responses in two fish species: inhibition in cunners (Tautogolabrus adspersus) and enhancement in striped bass (Morone saxatilis)
Vet. Immunol. Immunopathol.
(1986)- et al.
Development and characterisation of monoclonal antibodies against sea bass immunoglobulins Dicentrarchus labrax Linnaeus, 1758
Fish Shellfish Immunol.
(1995) Immunological indicators of environmental stress on immune protection and disease outbreaks
Am. Fish. Soc. Symp.
(1990)Acute toxicity of unionised ammonia to fingerling coho salmon
Progress Fish Cult.
(1978)- et al.
Serum protein changes in brown trout (Salmo trutta L.) after single injections of soluble and cellular antigens
J. Fish Biol.
(1977) - et al.
Chronic toxicity of ammonia for European sea bass (Dicentrarchus labrax) juveniles
Cited by (10)
Alterations in hematological and biochemical parameters, oxidative stress, and immune response in Takifugu rubripes under acute ammonia exposure
2021, Comparative Biochemistry and Physiology Part - C: Toxicology and PharmacologyCitation Excerpt :In the present study, a remarkable reduction in the serum TP and Alb levels was observed in fish exposed to ammonia. These results were consistent with those previously reported for Cirrhinus mrigala, Dicentrarchus labrax, and Pelteobagrus fulvidraco (Curdacier and Dutto, 1999; Das et al., 2015; Qi et al., 2017). Therefore, it is quite logical to suggest that renal excretion or proteolysis may be the main reason for the decrease in serum protein when the fish were exposed to increased ammonia concentrations.
Effect of ammonia-N on histology and expression of immunoglobulin M and component C3 in the spleen and head kidney of Pelteobagrus vachellii
2017, Aquaculture ReportsCitation Excerpt :Transcription of IgM in mandarin fish (Siniperca chuuatsi) in the head kidney and spleen were rapidly altered following exposure to Flavobacterium columnare (Tian et al., 2009), and was the case in turbot (Scophthalmus maximus) following exposure to Vibrio anguillarum (Gao et al., 2014). In contrast, in the present study, exposure to 1 and 5 mg/L ammonia resulted in an initial increase in IgM expression 6–12 h after treatment in P. vachellii, followed by a decrease at 24–96 h in both spleen and head kidney, and levels remained below untreated controls at 96 h. Similarly, the serum Ig concentration in sea bass (Dicentrarchus labrax) was 1.76 ± 0.43 and 1.19 ± 0.33 mg/L, significantly lower than the control group (3.39 ± 1.01 mg/mL) after 21 days of chronic ammonia exposure (Coeurdacier and Dutto, 1999). These results suggest that ammonia compromises the adaptive capability, unlike other stresses such as immunogens that induce IgM expression.
The effect of density on sea bass (Dicentrarchus labrax) performance in a tank-based recirculating system
2009, Aquacultural EngineeringBlood biochemistry profile of Qihe crucian carp Carassius auratus in different aquaponic systems
2020, Environmental Science and Pollution ResearchSalinity tolerance of Pangasianodon hypophthalmus in inland saline water: Effect on growth, survival and haematological parameters
2017, Ecology, Environment and ConservationIs total serum protein a good indicator for welfare in reared sea bass (Dicentrarchus labrax)?
2011, Aquatic Living Resources