Exceptional CO<sub>2</sub>Tolerance in White Sturgeon (<i>Acipenser transmontanus</i>) Is Associated with Protection of Maximum Cardiac Performance during Hypercapnia In Situ

Journal of Experimental Biology

Crossley

Kohl

et al. 2016

Self Cite

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.

Section: Cardiovascular Function May Be Protected By Preferential Ph supporting

confidence: 77%

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

Journal of Experimental Biology

Crossley

Kohl

et al. 2016

Self Cite

“…Why preferential pH i regulation was not retained more broadly can only be speculated upon at this time. Although preferential pH i regulation may be metabolically less costly than coupled pH regulation (Baker and Brauner, 2012) and protects cardiac performance during acute hypercarbia exposure (Baker et al, 2011;Hanson et al, 2009;Shartau et al, 2016), there may be unquantified long-term costs associated with preferential pH i regulation. This premise remains to be investigated.…”

Section: Preferential Ph I Regulation During Developmentmentioning

confidence: 99%

Preferential intracellular pH regulation: hypotheses and perspectives

Journal of Experimental Biology

Baker

Crossley

et al. 2016

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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.

“…Recent studies, however, have elucidated a different pattern in some species where pH I is tightly regulated despite large reductions in pH E , termed preferential pH I regulation (Brauner & Baker, ). This trait is best described in the white sturgeon Acipenser transmontanus Richardson 1836, a basal water‐breathing actinopterygian (Baker et al , , ; Huynh et al , ; Baker & Brauner, ). When A .…”

Section: Acid–base Balancementioning

confidence: 99%

“…transmontanus are subjected to a severe respiratory acidosis by means of hypercarbia (6% CO 2 ), pH E is depressed from 7·8 to 7·1 and is not compensated over 48 h (Baker et al , ). pH I of heart, muscle, brain, liver and white muscle, however, remain tightly regulated with no measurable depression, and more often a significant increase of up to 0·2 pH units within hours or days of exposure (Baker et al , , ). Preferential pH I regulation has now been documented in five bimodal species, the marbled swamp eel Synbranchus marmoratus Bloch 1795 (Heisler, ; also see Table ), P .…”

Section: Acid–base Balancementioning

confidence: 99%

Acid–base and ion balance in fishes with bimodal respiration

Journal of Fish Biology

Brauner

2014

The evolution of air breathing during the Devonian provided early fishes with bimodal respiration with a stable O2 supply from air. This was, however, probably associated with challenges and trade-offs in terms of acid-base balance and ionoregulation due to reduced gill:water interaction and changes in gill morphology associated with air breathing. While many aspects of acid-base and ionoregulation in air-breathing fishes are similar to water breathers, the specific cellular and molecular mechanisms involved remain largely unstudied. In general, reduced ionic permeability appears to be an important adaptation in the few bimodal fishes investigated but it is not known if this is a general characteristic. The kidney appears to play an important role in minimizing ion loss to the freshwater environment in the few species investigated, and while ion uptake across the gut is probably important, it has been largely unexplored. In general, air breathing in facultative air-breathing fishes is associated with an acid-base disturbance, resulting in an increased partial pressure of arterial CO2 and a reduction in extracellular pH (pHE ); however, several fishes appear to be capable of tightly regulating tissue intracellular pH (pHI ), despite a large sustained reduction in pHE , a trait termed preferential pHI regulation. Further studies are needed to determine whether preferential pHI regulation is a general trait among bimodal fishes and if this confers reduced sensitivity to acid-base disturbances, including those induced by hypercarbia, exhaustive exercise and hypoxia or anoxia. Additionally, elucidating the cellular and molecular mechanisms may yield insight into whether preferential pHI regulation is a trait ultimately associated with the early evolution of air breathing in vertebrates.