Morphometric and Enzymatic Changes in Gills of Rainbow Trout After Exposure to Elevated Temperature-Indications for Gill Remodeling

Overview

Journal Animals (Basel)

Date 2024 Mar 28

PMID 38540017

Authors

Franz Lahnsteiner

Affiliations

Soon will be listed here.

Abstract

Seven-month-old rainbow trout acclimated to 9 °C were used. The fish were gradually adapted to a water temperature of 20 °C over a period of seven days and then exposed to this temperature for 32 days. Changes in gill morphometry and histology and in enzyme activities in comparison to fish kept at 9 °C were investigated. No histopathological abnormalities were discerned at the heightened temperature. The gill epithelium thickened by approximately 40%, suggesting an increase in the branchial diffusion barrier for ions, water, and gases. Concurrently, there was a significant decrease in the activities of gill H-ATPase and Na/K-ATPase, indicative of a reduction in osmoregulation under elevated temperatures. Carbonic anhydrase activity exhibited an increase following the 32-day exposure to 20 °C, potentially mitigating the adverse effects of increased gill epithelium thickness on gaseous exchange. There were no indications of gill surface enlargement as the measurements of the length of the primary and secondary lamellae, as well as of the distances between them, were similar at 9 and 20 °C. The activities of the gill enzymes associated with glycolysis and the citric acid cycle displayed a varied response following the 32-day exposure of rainbow trout to 20 °C. Pyruvate kinase decreased, while lactate dehydrogenase increased, and malate dehydrogenase remained constant. This might suggest a decrease in the glycolytic rate, a greater reliance on anaerobic pathways at 20 °C compared to 9 °C, and the consistent efficiency of the citric acid cycle in the gills of rainbow trout in response to elevated temperatures. In summation, the data suggest a remodeling of rainbow trout gills in response to elevated temperatures, affecting both morphometric and metabolic aspects.

References

Alfonso S, Gesto M, Sadoul B . Temperature increase and its effects on fish stress physiology in the context of global warming. J Fish Biol. 2020; 98(6):1496-1508. DOI: 10.1111/jfb.14599. View

Bystriansky J, Schulte P . Changes in gill H+-ATPase and Na+/K+-ATPase expression and activity during freshwater acclimation of Atlantic salmon (Salmo salar). J Exp Biol. 2011; 214(Pt 14):2435-42. DOI: 10.1242/jeb.050633. View

Bowden A, Gardiner N, Couturier C, Stecyk J, Nilsson G, Munday P . Alterations in gill structure in tropical reef fishes as a result of elevated temperatures. Comp Biochem Physiol A Mol Integr Physiol. 2014; 175:64-71. PMC: 4452294. DOI: 10.1016/j.cbpa.2014.05.011. View

Sollid J, Nilsson G . Plasticity of respiratory structures--adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol. 2006; 154(1-2):241-51. DOI: 10.1016/j.resp.2006.02.006. View

Mohamad S, Liew H, Zainuddin R, Rahmah S, Waiho K, Ghaffar M . High environmental temperature and low pH stress alter the gill phenotypic plasticity of Hoven's carp Leptobarbus hoevenii. J Fish Biol. 2021; 99(1):206-218. DOI: 10.1111/jfb.14712. View

Chadwick J, McCormick S . Upper thermal limits of growth in brook trout and their relationship to stress physiology. J Exp Biol. 2017; 220(Pt 21):3976-3987. DOI: 10.1242/jeb.161224. View

Fiedler S, Wunnemann H, Hofmann I, Theobalt N, Feuchtinger A, Walch A . A practical guide to unbiased quantitative morphological analyses of the gills of rainbow trout (Oncorhynchus mykiss) in ecotoxicological studies. PLoS One. 2020; 15(12):e0243462. PMC: 7725368. DOI: 10.1371/journal.pone.0243462. View

Evans D, Piermarini P, Choe K . The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev. 2004; 85(1):97-177. DOI: 10.1152/physrev.00050.2003. View

Fowles J, Green H, Ouyang J . Na+-K+-ATPase in rat skeletal muscle: content, isoform, and activity characteristics. J Appl Physiol (1985). 2003; 96(1):316-26. DOI: 10.1152/japplphysiol.00745.2002. View

10.

LOWRY O, ROSEBROUGH N, FARR A, RANDALL R . Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. View

11.

Lahnsteiner F . Seasonal differences in thermal stress susceptibility of diploid and triploid brook trout, Salvelinus fontinalis (Teleostei, Pisces). J Fish Biol. 2022; 101(1):276-288. DOI: 10.1111/jfb.15118. View

12.

Rombough P . The functional ontogeny of the teleost gill: which comes first, gas or ion exchange?. Comp Biochem Physiol A Mol Integr Physiol. 2007; 148(4):732-42. DOI: 10.1016/j.cbpa.2007.03.007. View

13.

Gilmour K . New insights into the many functions of carbonic anhydrase in fish gills. Respir Physiol Neurobiol. 2012; 184(3):223-30. DOI: 10.1016/j.resp.2012.06.001. View

14.

Seidelin M, Brauner C, Jensen F, Madsen S . Vacuolar-type H(+)-ATPase and Na+, K(+)-ATPase expression in gills of Atlantic salmon (Salmo salar) during isolated and combined exposure to hyperoxia and hypercapnia in fresh water. Zoolog Sci. 2002; 18(9):1199-205. DOI: 10.2108/zsj.18.1199. View

15.

Tahar A, Kennedy A, Fitzgerald R, Clifford E, Rowan N . Longitudinal evaluation of the impact of traditional rainbow trout farming on receiving water quality in Ireland. PeerJ. 2018; 6:e5281. PMC: 6063216. DOI: 10.7717/peerj.5281. View

16.

Wood C, Eom J . The osmorespiratory compromise in the fish gill. Comp Biochem Physiol A Mol Integr Physiol. 2021; 254:110895. DOI: 10.1016/j.cbpa.2021.110895. View

17.

Nilsson G, Dymowska A, Stecyk J . New insights into the plasticity of gill structure. Respir Physiol Neurobiol. 2012; 184(3):214-22. DOI: 10.1016/j.resp.2012.07.012. View

18.

Sollid J, Weber R, Nilsson G . Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol. 2005; 208(Pt 6):1109-16. DOI: 10.1242/jeb.01505. View

19.

Islam S, Zahangir M, Ashaf-Ud-Doulah M, Khatun M, Shahjahan M . Extreme warm acclimation temperature alters oxygen consumption, micronucleus formation in erythrocytes, and gill morphology of rohu (Labeo rohita) fingerlings. Fish Physiol Biochem. 2020; 46(6):2323-2330. DOI: 10.1007/s10695-020-00886-6. View

20.

Gilmour K, Perry S . Conflict and Compromise: Using Reversible Remodeling to Manage Competing Physiological Demands at the Fish Gill. Physiology (Bethesda). 2018; 33(6):412-422. DOI: 10.1152/physiol.00031.2018. View