Anti-oxidative defences are modulated differentially in three freshwater teleosts in response to ammonia-induced oxidative stress

PLoS One. 2014 Apr 16;9(4):e95319. doi: 10.1371/journal.pone.0095319. eCollection 2014.

Abstract

Oxidative stress and the antioxidant response induced by high environmental ammonia (HEA) were investigated in the liver and gills of three freshwater teleosts differing in their sensitivities to ammonia. The highly ammonia-sensitive salmonid Oncorhynchus mykiss (rainbow trout), the less ammonia sensitive cyprinid Cyprinus carpio (common carp) and the highly ammonia-resistant cyprinid Carassius auratus (goldfish) were exposed to 1 mM ammonia (as NH4HCO3) for 0 h (control), 3 h, 12 h, 24 h, 48 h, 84 h and 180 h. Results show that HEA exposure increased ammonia accumulation significantly in the liver of all the three fish species from 24 h-48 h onwards which was associated with an increment in oxidative stress, evidenced by elevation of xanthine oxidase activity and levels of hydrogen peroxide (H2O2) and malondialdehyde (MDA). Unlike in trout, H2O2 and MDA accumulation in carp and goldfish liver was restored to control levels (84 h-180 h); which was accompanied by a concomitant increase in superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase activity and reduced ascorbate content. Many of these defence parameters remained unaffected in trout liver, while components of the glutathione redox cycle (reduced glutathione, glutathione peroxidase and glutathione reductase) enhanced to a greater extent. The present findings suggest that trout rely mainly on glutathione dependent defensive mechanism while carp utilize SOD, CAT and ascorbate as anti-oxidative sentinels. Hepatic cells of goldfish appear to utilize each of these protective systems, and showed more effective anti-oxidative compensatory responses towards HEA than carp, while trout were least effective. The present work also indicates that HEA exposure resulted in a relatively mild oxidative stress in the gills of all three species. This probably explains the almost complete lack of anti-oxidative responses in branchial tissue. This research suggests that oxidative stress, as well as the antioxidant potential clearly differ between salmonid and cyprinid species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological*
  • Ammonia / toxicity*
  • Animals
  • Ascorbate Peroxidases / genetics
  • Ascorbate Peroxidases / metabolism
  • Carps / genetics
  • Carps / metabolism*
  • Catalase / genetics
  • Catalase / metabolism
  • Gene Expression Regulation / drug effects
  • Gills / drug effects*
  • Gills / metabolism
  • Glutathione / metabolism
  • Glutathione Peroxidase / genetics
  • Glutathione Peroxidase / metabolism
  • Glutathione Reductase / genetics
  • Glutathione Reductase / metabolism
  • Goldfish / genetics
  • Goldfish / metabolism*
  • Hydrogen Peroxide / metabolism
  • Liver / drug effects*
  • Liver / metabolism
  • Malondialdehyde / metabolism
  • Oncorhynchus mykiss / genetics
  • Oncorhynchus mykiss / metabolism*
  • Oxidative Stress
  • Species Specificity
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Xanthine Oxidase / genetics
  • Xanthine Oxidase / metabolism

Substances

  • Malondialdehyde
  • Ammonia
  • Hydrogen Peroxide
  • Ascorbate Peroxidases
  • Catalase
  • Glutathione Peroxidase
  • Superoxide Dismutase
  • Xanthine Oxidase
  • Glutathione Reductase
  • Glutathione

Grants and funding

This work was supported by the Fonds Wetenschappelijk Onderzoek - Vlaanderen [FWO 1121310N]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.