Preferential intracellular pH regulation represents a general pattern of pH homeostasis during acid–base disturbances in the armoured catfish, Pterygoplichthys pardalis

The regulation of vertebrate acid-base balance during acute episodes of elevated internal P CO2 is typically characterized by extracellular pH ( pH e ) regulation. Changes in pH e are associated with qualitatively similar changes in intracellular tissue pH ( pH i ) as the two are typically coupled, referred to as 'coupled pH regulation'. However, not all vertebrates rely on coupled pH regulation; instead, some preferentially regulate pH i against severe and maintained reductions in pH e . Preferential pH i regulation has been identified in several adult fish species and an aquatic amphibian, but never in adult amniotes. Recently, common snapping turtles were observed to preferentially regulate pH i during development; the pattern of acid-base regulation in these species shifts from preferential pH i regulation in embryos to coupled pH regulation in adults. In this Commentary, we discuss the hypothesis that preferential pH i regulation may be a general strategy employed by vertebrate embryos in order to maintain acid-base homeostasis during severe acute acid-base disturbances. In adult vertebrates, the retention or loss of preferential pH i regulation may depend on selection pressures associated with the environment inhabited and/or the severity of acid-base regulatory challenges to which they are exposed. We also consider the idea that the retention of preferential pH i regulation into adulthood may have been a key event in vertebrate evolution, with implications for the invasion of freshwater habitats, the evolution of air breathing and the transition of vertebrates from water to land.

Section: Preferential Ph I Regulation In Adult Vertebratesmentioning

confidence: 99%

Section: Preferential Ph I Regulation During Developmentmentioning

confidence: 99%

Preferential intracellular pH regulation: hypotheses and perspectives

Shartau

Baker

Crossley

et al. 2016

“…The 'bicarbonate concentration threshold', originally described by Heisler (Heisler, 1984;Heisler et al, 1982), limits plasma [HCO 3 − ] uptake to approximately 27-33 mmol l −1 , which limits complete pH e compensation to CO 2 tensions below ∼2-2.5 kPa P CO2 ). In addition to conferring exceptional tolerance to hypercarbia-induced acidosis, preferential pH i regulation appears to play a role in short-term pH i regulation during metabolic acidosis, metabolic alkalosis (Harter et al, 2014) and respiratory alkalosis (Fig. 5).…”

Section: Acid-base Regulation During Developmentmentioning

confidence: 99%

“…This pattern of coupled pH i and pH e recovery following a respiratory acidosis is thought to be representative of vertebrates in general. However, in CO 2 -tolerant fishes, it is becoming increasingly clear that pH i in a number of species is tightly regulated in the complete absence of pH e regulation (Baker et al, 2009a;Brauner and Baker, 2009;Brauner et al, 2004;Harter et al, 2014;Heisler, 1982;Shartau and Brauner, 2014), termed preferential pH i regulation. Preferential pH i regulation confers exceptional CO 2 tolerance by allowing animals to withstand severe acid-base disturbances Shartau and Brauner, 2014).…”

Section: Introductionmentioning

confidence: 99%

Embryonic common snapping turtles (Chelydra serpentina) preferentially regulate intracellular tissue pH during acid-base challenges

Shartau

Crossley

Kohl

et al. 2016

The nests of embryonic turtles naturally experience elevated CO 2 (hypercarbia), which leads to increased blood P CO2 and a respiratory acidosis, resulting in reduced blood pH [extracellular pH ( pH e )]. Some fishes preferentially regulate tissue pH [intracellular pH ( pH i )] against changes in pH e ; this has been proposed to be associated with exceptional CO 2 tolerance and has never been identified in amniotes. As embryonic turtles may be CO 2 tolerant based on nesting strategy, we hypothesized that they preferentially regulate pH i , conferring tolerance to severe acute acid-base challenges. This hypothesis was tested by investigating pH regulation in common snapping turtles (Chelydra serpentina) reared in normoxia then exposed to hypercarbia (13 kPa P CO2 ) for 1 h at three developmental ages: 70% and 90% of incubation, and yearlings. Hypercarbia reduced pH e but not pH i , at all developmental ages. At 70% of incubation, pH e was depressed by 0.324 pH units while pH i of brain, white muscle and lung increased; heart, liver and kidney pH i remained unchanged. At 90% of incubation, pH e was depressed by 0.352 pH units but heart pH i increased with no change in pH i of other tissues. Yearlings exhibited a pH e reduction of 0.235 pH units but had no changes in pH i of any tissues. The results indicate common snapping turtles preferentially regulate pH i during development, but the degree of response is reduced throughout development. This is the first time preferential pH i regulation has been identified in an amniote. These findings may provide insight into the evolution of acid-base homeostasis during development of amniotes, and vertebrates in general.

“…It has therefore been suggested that the reduced surface area of the gills of air-breathing fishes places limitations on transepithelial ion exchange, thus constraining the branchial capacity for acid-base regulation (Brauner and Baker, 2009;Shartau and Brauner, 2014). Therefore, all studies on acid-base regulation in air-breathing fishes to date indicate a low capacity for exchange of acid-base equivalents in pH e regulation and a preferential regulation of intracellular pH, during a respiratory acidosis (Brauner and Baker, 2009;Brauner et al, 2004;Harter et al, 2014b;Heisler, 1982;Shartau and Brauner, 2014).…”

Section: Introductionmentioning

confidence: 99%

High capacity for extracellular acid-base regulation in the air-breathing fishPangasianodon hypophthalmus

Damsgaard

Gam

Tuong

et al. 2015

The evolution of accessory air-breathing structures is typically associated with reduction of the gills, although branchial ion transport remains pivotal for acid-base and ion regulation. Therefore, airbreathing fishes are believed to have a low capacity for extracellular pH regulation during a respiratory acidosis. In the present study, we investigated acid-base regulation during hypercapnia in the airbreathing fish Pangasianodon hypophthalmus in normoxic and hypoxic water at 28-30°C. Contrary to previous studies, we show that this air-breathing fish has a pronounced ability to regulate extracellular pH (pH e ) during hypercapnia, with complete metabolic compensation of pH e within 72 h of exposure to hypoxic hypercapnia with CO 2 levels above 34 mmHg. The high capacity for pH e regulation relies on a pronounced ability to increase levels of HCO 3 − in the plasma. Our study illustrates the diversity in the physiology of air-breathing fishes, such that generalizations across phylogenies may be difficult.