Preferential intracellular pH regulation is a common trait amongst fishes exposed to high environmental CO2

Abstract

Acute (<96 h) exposure to elevated environmental CO 2 (hypercarbia) induces a pH disturbance in fishes that is often compensated by concurrent recovery of intracellular and extracellular pH (pH i and pH e , respectively; coupled pH regulation). However, coupled pH regulation may be limited at CO 2 partial pressure (P CO2) tensions far below levels that some fishes naturally encounter. Previously, four hypercarbiatolerant fishes had been shown to completely and rapidly regulate heart, brain, liver and white muscle pH i during acute exposure to >4 kPa P CO2 (preferential pH i regulation) before pH e compensation was observed. Here, we test the hypothesis that preferential pH i regulation is a widespread strategy of acid-base regulation among fish by measuring pH i regulation in 10 different fish species that are broadly phylogenetically separated, spanning six orders, eight families and 10 genera. Contrary to previous views, we show that preferential pH i regulation is the most common strategy for acid-base regulation within these fishes during exposure to severe acute hypercarbia and that this strategy is associated with increased hypercarbia tolerance. This suggests that preferential pH i regulation may confer tolerance to the respiratory acidosis associated with hypercarbia, and we propose that it is an exaptation that facilitated key evolutionary transitions in vertebrate evolution, such as the evolution of air breathing.

Rapid blood acid–base regulation by European sea bass (Dicentrarchus labrax) in response to sudden exposure to high environmental CO2

“…Haemoglobins (Hb) of fish species show strong Bohr and Root effects ( Wells, 2009 ) which reduce Hb–O 2 binding affinity and the O 2 carrying capacity when erythrocyte intracellular pH (pH i ) decreases. While fish have adaptations to regulate pH i of erythrocytes ( Cossins and Richardson, 1985 ; Nikinmaa and Tufts, 1989 ; Thomas and Perry, 1992 ), erythrocyte pH i in many fish species (particularly marine fish) is closely linked to whole-blood pH ( Brauner and Baker, 2009 ; Shartau et al, 2020 ). Therefore, adaptations which enhance the speed of whole-blood acid–base regulation will also provide faster restoration of O 2 transport capacity and minimise disruption to energetically expensive activities such as foraging and digestion.…”

Evolutionary links between intra‐ and extracellular acid–base regulation in fish and other aquatic animals

“…In addition to sturgeon, preferential pHi regulation has been observed in a number of other fishes including the armored catfish (Pterygoplichthys pardalis), the marbled swamp eel (Synbranchus marmoratus), the striped catfish (Pangasianodon hypophthalmus), and three species of gar (Lepisosteus oculatus, L. osseus, and Atractosteus spatula) (reviewed in Shartau et al, 2020). Preferential pHi regulation was also observed in the late stage developing embryos of the common snapping turtle (Chelydra serpentine; Shartau, Crossley, Kohl, & Brauner, 2016) and American alligator (Alligator mississippiensis; Shartau, Crossley, Kohl, Elsey, & Brauner, 2018).…”

Endosymbiont strategic shifts inhibit cooperation during coral bleaching recovery

“…Corals might thus prioritize maintaining pH i at the expense of pH ECM during bleaching recovery, perhaps by altering protein expression or localization of different ion transporters [68], obscuring any individual-level differences in total pH regulatory capacity. This sort of ‘preferential pH regulation’ has been observed in air-breathing fishes that rapidly regulate pH i in response to CO 2 stress while allowing extracellular pH to remain acidic [69, 70]. Further research into the relationship between coral pH i and calcification should test the possibility that cnidarians also use preferential pH i regulation to balance the multiple acid-base challenges they face, including endosymbiont photosynthesis, cellular respiration, environmental acidification, and calcification [39].…”