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ABSTRACT The gill is the primary site of ionoregulation and gas exchange in adult teleost fishes. However, those characteristics that benefit diffusive gas exchange (large, thin gills) may also enhance the passive equilibration of ions and water that threaten osmotic homeostasis. Our literature review revealed that gill surface area and thickness were similar in freshwater (FW) and seawater (SW) species; however, the diffusive oxygen (O2) conductance (Gd) of the gill was lower in FW species. While a lower Gd may reduce ion losses, it also limits O2 uptake capacity and possibly aerobic performance in situations of high O2 demand (e.g. exercise) or low O2 availability (e.g. environmental hypoxia). We also found that FW fishes had significantly higher haemoglobin (Hb)–O2 binding affinities than SW species, which will increase the O2 diffusion gradient across the gills. Therefore, we hypothesized that the higher Hb–O2 affinity of FW fishes compensates, in part, for their lower Gd. Using a combined literature review and modelling approach, our results show that a higher Hb–O2 affinity in FW fishes increases the flux of O2 across their low-Gd gills. In addition, FW and SW teleosts can achieve similar maximal rates of O2 consumption (ṀO2,max) and hypoxia tolerance (Pcrit) through different combinations of Hb–O2 affinity and Gd. Our combined data identified novel patterns in gill and Hb characteristics between FW and SW fishes and our modelling approach provides mechanistic insight into the relationship between aerobic performance and species distribution ranges, generating novel hypotheses at the intersection of cardiorespiratory and ionoregulatory fish physiology. 

White seabass ( Atractoscion nobilis) increasingly experience periods of low oxygen (O 2 ; hypoxia) and high carbon dioxide (CO 2 , hypercapnia) due to climate change and eutrophication of the coastal waters of California. Hemoglobin (Hb) is the principal O 2 carrier in the blood and in many teleost fishes Hb-O 2 binding is compromised at low pH; however, the red blood cells (RBC) of some species regulate intracellular pH with adrenergically stimulated sodium-proton-exchangers (β-NHEs). We hypothesized that RBC β-NHEs in white seabass are an important mechanism that can protect the blood O 2 -carrying capacity during hypoxia and hypercapnia. We determined the O 2 -binding characteristics of white seabass blood, the cellular and subcellular response of RBCs to adrenergic stimulation, and quantified the protective effect of β-NHE activity on Hb-O 2 saturation. White seabass had typical teleost Hb characteristics, with a moderate O 2 affinity (Po 2 at half-saturation; P 50 2.9 kPa) that was highly pH-sensitive (Bohr coefficient −0.92; Root effect 52%). Novel findings from super-resolution microscopy revealed β-NHE protein in vesicle-like structures and its translocation into the membrane after adrenergic stimulation. Microscopy data were corroborated by molecular and phylogenetic results and a functional characterization of β-NHE activity. The activation of RBC β-NHEs increased Hb-O 2 saturation by ∼8% in normoxic hypercapnia and by up to ∼20% in hypoxic normocapnia. Our results provide novel insight into the cellular mechanism of adrenergic RBC stimulation within an ecologically relevant context. β-NHE activity in white seabass has great potential to protect arterial O 2 transport during hypoxia and hypercapnia but is less effective during combinations of these stressors. 

Previously, we showed that the evolution of high acuity vision in fishes was directly associated with their unique pH-sensitive hemoglobins that allow O 2 to be delivered to the retina at PO 2 s more than ten-fold that of arterial blood (Damsgaard et al., 2019). Here, we show strong evidence that vacuolar-type H + -ATPase and plasma-accessible carbonic anhydrase in the vascular structure supplying the retina act together to acidify the red blood cell leading to O 2 secretion. In vivo data indicate that this pathway primarily affects the oxygenation of the inner retina involved in signal processing and transduction, and that the evolution of this pathway was tightly associated with the morphological expansion of the inner retina. We conclude that this mechanism for retinal oxygenation played a vital role in the adaptive evolution of vision in teleost fishes. 

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.