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ABSTRACT Fish in coastal ecosystems can be exposed to acute variations in CO2 of between 0.2 and 1 kPa CO2 (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 CO2 (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 CO2, European sea bass (Dicentrarchus labrax) completely regulate erythrocyte intracellular pH within ∼40 min, thus restoring haemoglobin–O2 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 HCO3− 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 CO2 exposure occurred in seawater with experimentally reduced HCO3− 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 CO2 fluctuations that naturally occur in coastal environments.
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Evolutionary links between intra- and extracellular acid-base regulation in fish and other aquatic animals
The acid–base relevant molecules carbon dioxide (CO2), protons (H+), and bicarbonate (HCO3−) are substrates and end products of some of the most essential physiological functions including aerobic and anaerobic respiration, ATP hydrolysis, photosynthesis, and calcification. The structure and function of many enzymes and other macromolecules are highly sensitive to changes in pH, and thus maintaining acid–base homeostasis in the face of metabolic and environmental disturbances is essential for proper cellular function. On the other hand, CO2, H+, and HCO3− have regulatory effects on various proteins and processes, both directly through allosteric modulation and indirectly through signal transduction pathways. Life in aquatic environments presents organisms with distinct acid–base challenges that are not found in terrestrial environments. These include a relatively high CO2 relative to O2 solubility that prevents internal CO2/HCO3 − accumulation to buffer pH, a lower O2 content that may favor anaerobic metabolism, and variable environmental CO2, pH and O2 levels that require dynamic adjustments in acid–base homeostatic mechanisms. Additionally, some aquatic animals purposely create acidic or alkaline microenvironments that drive specialized physiological functions. For example, acidifying mechanisms can enhance O2 delivery by red blood cells, lead to ammonia trapping for excretion or buoyancy purposes, or lead to CO2 accumulation to promote photosynthesis by endosymbiotic algae. On the other hand, alkalinizing mechanisms can serve to promote calcium carbonate skeletal formation. This nonexhaustive review summarizes some of the distinct acid–base homeostatic mechanisms that have evolved in aquatic organisms to meet the particular challenges of this environment.
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- Award ID(s):
- 1754994
- PAR ID:
- 10156716
- Date Published:
- Journal Name:
- Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
- ISSN:
- 2471-5638
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1002/jez.2367
