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

Authors: ALLEN, PETER - Mississippi State University; SHARTAU, R - University Of British Columbia; BAKER, D - Vancouver Island University; HARTER, T - University Of British Columbia; ABOAGYE, D - Mississippi State University; VAL, A - Mississippi State University; CROSSLEY, D - University Of North Texas; KOHL, Z - University Of North Texas; HEDRICK, M - California State University; DAMSGAARD, C - University Of British Columbia; BRAUNER, C - University Of British Columbia

Submitted to: Journal of Experimental Biology Online, Vol 3
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/25/2020
Publication Date: 4/1/2020
Citation: Allen, P.J., Shartau, R.B., Baker, D.W., Harter, T.S., Aboagye, D.L., Val, A.L., Crossley, D.A., Kohl, Z.F., Hedrick, M.S., Damsgaard, C., Brauner, C.J. 2020. Preferential intracellular pH regulation is a common trait amongst fishes exposed to high environmental CO2. Journal of Experimental Biology Online, Vol 3. 223:jeb20886. https://doi.org/10.1242/jeb.208868.
DOI: https://doi.org/10.1242/jeb.208868

Interpretive Summary: Fish are frequently subjected to high carbon dioxide environments in aquaculture. This study compared representative species from different groups of fishes to better understand physiological systems used to compensate for high environmental carbon dioxide.

Technical Abstract: Acute (<96 h) exposure to elevated environmental CO2 (hypercarbia) induces a pH disturbance in fishes that is often compensated by concurrent recovery of intracellular and extracellular pH (pHi and pHe, respectively; coupled pH regulation). However, coupled pH regulation may be limited at CO2 partial pressure (PCO2) tensions far below levels that some fishes naturally encounter. Previously, four hypercarbia tolerant fishes had been shown to completely and rapidl regulate heart, brain, liver and white muscle pHi during acute exposure to>4 kPa PCO2 (preferential pHi regulation) before pHe compensation was observed. Here, we test the hypothesis that preferential pHi regulation is a widespread strategy of acid–base regulation among fish by measuring pHi 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 pHi 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 pHi regulation may confer tolerance to the respiratory acidosis associated with hypercarbia, and we propose that it is an exaptation that facilitated key evolutionary transitions invertebrate evolution, such as the evolution of air breathing.