Rapid blood acid–base regulation by European sea bass ( Dicentrarchus labrax) in response to sudden exposure to high environmental CO ₂

ABSTRACT

Fish in coastal ecosystems can be exposed to acute variations in CO ₂ of between 0.2 and 1 kPa CO ₂ (2000–10,000 µatm). Coping with this environmental challenge will depend on the ability to rapidly compensate for the internal acid–base disturbance caused by sudden exposure to high environmental CO ₂ (blood and tissue acidosis); however, studies about the speed of acid–base regulatory responses in marine fish are scarce. We observed that upon sudden exposure to ∼1 kPa CO ₂, European sea bass ( Dicentrarchus labrax) completely regulate erythrocyte intracellular pH within ∼40 min, thus restoring haemoglobin–O ₂ affinity to pre-exposure levels. Moreover, blood pH returned to normal levels within ∼2 h, which is one of the fastest acid–base recoveries documented in any fish. This was achieved via a large upregulation of net acid excretion and accumulation of HCO ₃ ⁻ in blood, which increased from ∼4 to ∼22 mmol l ⁻¹. While the abundance and intracellular localisation of gill Na ⁺/K ⁺-ATPase (NKA) and Na ⁺/H ⁺ exchanger 3 (NHE3) remained unchanged, the apical surface area of acid-excreting gill ionocytes doubled. This constitutes a novel mechanism for rapidly increasing acid excretion during sudden blood acidosis. Rapid acid–base regulation was completely prevented when the same high CO ₂ exposure occurred in seawater with experimentally reduced HCO ₃ ⁻ and pH, probably because reduced environmental pH inhibited gill H ⁺ excretion via NHE3. The rapid and robust acid–base regulatory responses identified will enable European sea bass to maintain physiological performance during large and sudden CO ₂ fluctuations that naturally occur in coastal environments.

Abstract

Summary: European sea bass exposed to 1 kPa (10,000 µatm) CO ₂ regulate blood and red cell pH within 2 h and 40 min, respectively, protecting O ₂ transport capacity, via enhanced gill acid excretion.