The role of carbonic anhydrase-mediated tissue oxygen extraction in a marine teleost acclimated to hypoxia

With the growing prevalence of hypoxia (O-2 levels <= 2 mg l(-1)) in aquatic and marine ecosystems, there is increasing interest in the adaptive mechanisms fish may employ to better their performance in stressful environments. Here, we investigated the contribution of a proposed strategy for enhancing tissue O-2 extraction - plasma -accessible carbonic anhydrase (CA-IV) - under hypoxia in a species of estuarine fish (red drum, Sciaenops ocellatus) that thrives in fluctuating habitats. We predicted that hypoxia-acclimated fish would increase the prevalence of CA-IV in aerobically demanding tissues to confer more efficient tissue O-2 extraction. Furthermore, we predicted the phenotypic changes to tissue O-2 extraction that occur with hypoxia acclimation may improve respiratory and swim performance under 100% O-2 conditions (i.e. normoxia) when compared with performance in fish that have not been acclimated to hypoxia. Interestingly, there were no significant differences in relative CA-IV mRNA expression, protein abundance or enzyme activity between the two treatments, suggesting CA-IV function is maintained under hypoxia. Likewise, respiratory performance of hypoxia-acclimated fish was similar to that of control fish when tested in normoxia. Critical swim speed (Licrit) was significantly higher in hypoxia-acclimated fish but translated to marginal ecological benefits with an increase of similar to 0.3 body lengths per second. Instead, hypoxia-acclimated fish may have relied more heavily on anaerobic metabolism during their swim trials, utilizing burst swimming 1.5 times longer than control fish. While the maintenance of CA-IV may still be an important contributor for hypoxia tolerance, our evidence suggests hypoxia-acclimated red drum are using other mechanisms to cope in an O-2-depleted environment.

Automated summary

This study investigated the strategy of enhancing tissue oxygen extraction in red drum fish under hypoxia. The results showed that there were no significant increases in the expression and activity of carbonic anhydrase under hypoxia. Furthermore, the respiratory and swim performance of hypoxia-acclimated red drum fish was similar to the control fish in normoxia. However, the hypoxia-acclimated fish relied more on anaerobic metabolism during swim trials.