Carbonic anhydrase and acid–base regulation in fish

Gilmour, K. M.; Perry, Steve F.

doi:10.1242/jeb.029181

Cited by 180 publications

(135 citation statements)

References 176 publications

(313 reference statements)

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“…Although our understanding of the physiological significance of CA in acid-base/ionoregulation in fish is far from complete, putative roles of CA have been described in several species including zebrafish (for review, see Gilmour, 2012;Gilmour and Perry, 2009). Boisen et al (Boisen et al, 2003) reported that inhibition of CA with ethoxzolamide reduced Na + uptake in adult zebrafish acclimated to hard water, whereas it increased Na + uptake in fish acclimated to soft water.…”

Section: Carbonic Anhydrasementioning

confidence: 99%

“…The mechanisms of ionic and acid-base regulation in fish have been summarized in previous reviews (Claiborne et al, 2002;Evans et al, 2005;Gilmour and Perry, 2009;Goss et al, 1992;Haswell et al, 1980;Hwang, 2009;Marshall and Grosell, 2006;McDonald, 1983a;Perry, 1997;Perry and Gilmour, 2006;Wood, 1989). In this review we provide an overview of the general effects of acid exposure on FW fish, with particular emphasis on recent developments linking environmental acidification and ionic regulation in the acid-tolerant zebrafish.…”

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confidence: 98%

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The physiology of fish at low pH: the zebrafish as a model system

Kwong

Kumai

Perry

2014

Journal of Experimental Biology

117

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Ionic regulation and acid-base balance are fundamental to the physiology of vertebrates including fish. Acidification of freshwater ecosystems is recognized as a global environmental problem, and the physiological responses to acid exposure in a few fish species are well characterized. However, the underlying mechanisms promoting ionic and acid-base balance for most fish species that have been investigated remain unclear. Zebrafish (Danio rerio) has emerged as a powerful model system to elucidate the molecular basis of ionic and acid-base regulation. The utility of zebrafish is related to the ease with which it can be genetically manipulated, its suitability for state-of-the-art molecular and cellular approaches, and its tolerance to diverse environmental conditions. Recent studies have identified several key regulatory mechanisms enabling acclimation of zebrafish to acidic environments, including activation of the sodium/hydrogen exchanger (NHE) and H + -ATPase for acid secretion and Na + uptake, cortisol-mediated regulation of transcellular and paracellular Na + movements, and ionocyte proliferation controlled by specific cell-fate transcription factors. These integrated physiological responses ultimately contribute to ionic and acid-base homeostasis in zebrafish exposed to acidic water. In the present review, we provide an overview of the general effects of acid exposure on freshwater fish, the adaptive mechanisms promoting extreme acid tolerance in fishes native to acidic environments, and the mechanisms regulating ionic and acid-base balance during acid exposure in zebrafish. KEY WORDS: Acid exposure, Acid-base balance, Ionic regulation, Zebrafish IntroductionDeclining fish populations in acidified lakes and streams (see review by McDonald, 1983a) was a significant factor promoting intensive research over the past 40 years on the ecological and physiological consequences of aquatic acidification. In freshwater (FW) ecosystems, acidification is caused largely by atmospheric acidic deposition (i.e. acid rain). Acidification of FW is a global problem, which has been documented in several geographic regions including eastern Europe, the USA and China (Psenner, 1994;Schindler, 1988;Wright et al., 2005). In Canada, it is estimated that about 40% of lakes are in regions susceptible to acid deposition (Kelso et al., 1990). Most aquatic animals, including fish, live in a narrow range of pH near neutrality, and acute or chronic exposure to acidic water can adversely affect their physiological functions (McDonald, 1983a;Wood, 1989). Nevertheless, some species thrive in acidic environments, and thus can serve as useful models for investigating the mechanisms underlying adaptation to acid stress. REVIEWDepartment of Biology, University of Ottawa, 30 Marie Curie, Ottawa, ON, Canada, K1N 6N5.*Author for correspondence (wkwong@uottawa.ca)The mechanisms of ionic and acid-base regulation in fish have been summarized in previous reviews (Claiborne et al., 2002;Evans et al., 2005;Gilmour and Perry, 2009;Goss et al., 19...

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Section: Carbonic Anhydrasementioning

confidence: 99%

mentioning

confidence: 98%

The physiology of fish at low pH: the zebrafish as a model system

Kwong

Kumai

Perry

2014

Journal of Experimental Biology

117

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“…CA has been reported in the swim bladder of bowfin (Gervais and Tufts, 1998) and in fish muscle (for review, see Henry and Swenson, 2000). CAs are important in acid-base regulation in many sites including muscle, gills and kidney (Geers and Gros, 2000;Gilmour and Perry, 2009).Teleost fish RBCs have sodium/proton exchange (NHE) isoforms and a Band III anion exchange (AE) protein that take up sodium and chloride and excrete protons and bicarbonate, respectively ( Fig. 3) and are involved in volume regulation (Heming et al, 1986;Claiborne et al, 1999;Cossins and Gibson, 1997;Rummer and Brauner, 2011;Rummer et al, 2010;Weaver et al, 1999).…”

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confidence: 99%

A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes

Randall

Rummer

Wilson³

et al. 2014

Journal of Experimental Biology

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Teleost fishes constitute 95% of extant aquatic vertebrates, and we suggest that this is related in part to their unique mode of tissue oxygenation. We propose the following sequence of events in the evolution of their oxygen delivery system. First, loss of plasmaaccessible carbonic anhydrase (CA) in the gill and venous circulations slowed the Jacobs-Stewart cycle and the transfer of acid between the plasma and the red blood cells (RBCs). This ameliorated the effects of a generalised acidosis (associated with an increased capacity for burst swimming) on haemoglobin (Hb)-O 2 binding. Because RBC pH was uncoupled from plasma pH, the importance of Hb as a buffer was reduced. The decrease in buffering was mediated by a reduction in the number of histidine residues on the Hb molecule and resulted in enhanced coupling of O 2 and CO 2 transfer through the RBCs. In the absence of plasma CA, nearly all plasma bicarbonate ultimately dehydrated to CO 2 occurred via the RBCs, and chloride/bicarbonate exchange was the rate-limiting step in CO 2 excretion. This pattern of CO 2 excretion across the gills resulted in disequilibrium states for CO 2 hydration/dehydration reactions and thus elevated arterial and venous plasma bicarbonate levels. Plasma-accessible CA embedded in arterial endothelia was retained, which eliminated the localized bicarbonate disequilibrium forming CO 2 that then moved into the RBCs. Consequently, RBC pH decreased which, in conjunction with pH-sensitive Bohr/Root Hbs, elevated arterial oxygen tensions and thus enhanced tissue oxygenation. Counter-current arrangement of capillaries (retia) at the eye and later the swim bladder evolved along with the gas gland at the swim bladder. Both arrangements enhanced and magnified CO 2 and acid production and, therefore, oxygen secretion to those specialised tissues. The evolution of β-adrenergically stimulated RBC Na + /H + exchange protected gill O 2 uptake during stress and further augmented plasma disequilibrium states for CO 2 hydration/dehydration. Finally, RBC organophosphates (e.g. NTP) could be reduced during hypoxia to further increase Hb-O 2 affinity without compromising tissue O 2 delivery because high-affinity Hbs could still adequately deliver O 2 to the tissues via Bohr/Root shifts. We suggest that the evolution of this unique mode of tissue O 2 transfer evolved in the Triassic/Jurassic Period, when O 2 levels were low, ultimately giving rise to the most extensive adaptive radiation of extant vertebrates, the teleost fishes. IntroductionTeleost fishes comprise 95% of all extant fishes, with approximately 26,000 named species (Helfman et al., 1997). Teleosts first appeared in the early Triassic period 200-250 million years ago (MYA) and have since radiated into almost all aquatic environments (Nelson, 1994;Near et al., 2012). The ray-finned fishes, to which the teleost fishes belong, diverged from the lobe-finned fishes (e.g. lungfishes) around the Devonian, 400 MYA. The lobe-finned fishes were very successful until the Permian crisis 252 MYA...

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“…We also found an up-regulation of genes related to carbonic anhydrase activity. This enzyme has been implicated in ion regulation, carbon dioxide (CO 2 ) excretion, and acid base balance in the gills of euryhaline fish (Gilmour and Perry 2009;Gilmour 2012). Indeed, in all comparisons involving wild A. grahami, several isoforms of carbonic anhydrase were found, emphasizing the importance of this enzyme in the metabolism of this species under its native challenging environmental conditions in the wild (Table S5).…”

Section: Gene Expression Changes In a Grahamimentioning

confidence: 97%

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

et al. 2015

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The Magadi tilapia (Alcolapia grahami) is a cichlid fish that inhabits one of the Earth's most extreme aquatic environments, with high pH ( -10), salinity (-60 % of seawater), high temperatures ( -40 °C), and fluctuating oxygen regimes. The Magadi tilapia evolved several unique behavioral, physiological, and anatomical adaptations, some of which are constituent and thus retained in freshwater conditions. We conducted a transcriptomic analysis on A. grahami to study the evolutionary basis of tolerance to multiple stressors. To identify the adaptive regulatory changes associated with stress responses, we massively sequenced gill transcriptomes (RNAseq) from wild and freshwater-acclimated specimens of A. grahami. As a control, corresponding transcriptome data from Oreochromis leucostictus, a closely related freshwater species, were generated. We found expression differences in a large number of genes with known functions related to osmoregulation, energy metabolism, ion transport, and chemical detoxification. Over-representation of metabolism-related gene ontology terms in wild individuals compared to laboratory-acclimated specimens suggested that freshwater conditions greatly decrease the metabolic requirements of this species. Twenty-five genes with diverse physiological functions related to responses to water stress showed signs of divergent natural selection between the Magadi tilapia and its freshwater relative, which shared a most recent common ancestor only about four million years ago. The complete set of genes responsible for urea excretion was identified in the gill transcriptome of A. grahami, making it the only fish species to have a functional ornithine-urea cycle pathway in the gills a major innovation for increasing nitrogenous waste efficiency.

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Carbonic anhydrase and acid–base regulation in fish

Cited by 180 publications

References 176 publications

The physiology of fish at low pH: the zebrafish as a model system

The physiology of fish at low pH: the zebrafish as a model system

A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

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