Biochemical properties and immunohistochemical localization of carbonic anhydrase in the sacculus of the inner ear in the salmon Oncorhynchus masou (2023)


Teleost otoliths (sagittae) are calcium carbonate concretions and function as sound detection and gravity sensing organs (Lowenstein, 1971). They are an acellular tissue and grow in the closed sac of the sacculus without any direct contact to cells. The sacculus is filled with endolymph, which must contain all the precursors of otolith materials. Endolymph has a high concentration of bicarbonate and high alkalinity, compared with plasma, and is oversaturated with otolith minerals (Mugiya and Takahashi, 1985, Payan et al., 1997, Takagi, 1997, Takagi, 2002). These properties of the endolymph may be regulated by the local activity of carbonic anhydrase in the sacculus (Mugiya, 1977, Payan et al., 1997, Tohse and Mugiya, 2001). The sacculus consists of sensory, transitional and squamous epithelia each surrounded by a layer of the connective tissue (Saitoh and Yamada, 1989, Takagi, 1997).

Carbonic anhydrase (CA, EC, a catalyst for the conversion of CO2 to HCO3 and vice versa, is abundantly localized in the gill epithelium and erythrocytes in fish, and plays an essential role in respiratory function (Perry and Laurent, 1990). CA is also reported to be dually involved in biomineralization by supplying CO32− via bicarbonate dehydration to the site of CaCO3 deposition and/or by eliminating protons derived from carbonate formation. Egg shell calcification is facilitated through the action of HCO3-ATPase and CA in the epithelial cells of the shell gland (Nys and de Laage, 1984). CA was involved in supplying bicarbonate from CO2 derived from zooxanthellae in coral calcification (Marshall, 1996, Al-Moghrabi et al., 1996, Furla et al., 2000). Mugiya, 1977, Mugiya, 1986 reported that calcium deposition on otoliths was inhibited by acetazolamide, an inhibitor of CA. Moreover, Mugiya and Takahashi (1985) reported that acetazolamide induced acidification and an increase in total CO2 levels in both serum and endolymph. Payan et al. (1997) reported that CA was involved in maintaining the alkalinity in endolymph by transporting H+ from the sacculus to the blood. These results suggest that CA facilitates calcification by creating alkaline environment and by increasing bicarbonate concentrations in situ. However, the biochemical properties and localization of saccular CA are still unknown.

In this study, we examined the biochemical property of saccular CA by a chemical assay and Western blotting in salmon. Immunohistochemical localization was also examined.

Cited by (24)

  • Elucidating the acid-base mechanisms underlying otolith overgrowth in fish exposed to ocean acidification

    2022, Science of the Total Environment

    Citation Excerpt :

    The chemistry of the endolymph is actively controlled by the inner ear epithelium to maintain acid-base conditions that promote biomineralization, namely, higher pH, [HCO3−], [CO32−], and total CO2 than the blood (Payan et al., 1999, 1997; Takagi, 2002; Takagi et al., 2005). This gradient is actively maintained by two types of ion-transporting cells (“ionocytes”): the Type-I ionocyte, which transports K+ and Cl− into the endolymph and removes H+ powered by Na+/K+-ATPase (NKA) (Kwan et al., 2020; Mayer-Gostan et al., 1997; Payan et al., 1997; Takagi, 1997) and the Type-II ionocyte, which secretes HCO3− into the endolymph driven by V-type H+-ATPase (VHA) (Kwan et al., 2020; Mayer-Gostan et al., 1997; Payan et al., 1997; Takagi, 1997; Tohse et al., 2004, 2006). However numerous other cells within the inner ear organ also express NKA and VHA, including the sensory hair cells and the endothelial cells that make up the blood vessels (Kwan et al., 2020; Mayer-Gostan et al., 1997; Shiao et al., 2005).

    Over a decade ago, ocean acidification (OA) exposure was reported to induce otolith overgrowth in teleost fish. This phenomenon was subsequently confirmed in multiple species; however, the underlying physiological causes remain unknown. Here, we report that splitnose rockfish (Sebastes diploproa) exposed to ~1600 μatm pCO2 (pH ~7.5) were able to fully regulated the pH of both blood and endolymph (the fluid that surrounds the otolith within the inner ear). However, while blood was regulated around pH 7.80, the endolymph was regulated around pH ~8.30. These different pH setpoints result in increased pCO2 diffusion into the endolymph, which in turn leads to proportional increases in endolymph [HCO3] and [CO32]. Endolymph pH regulation despite the increased pCO2 suggests enhanced H+ removal. However, a lack of differences in inner ear bulk and cell-specific Na+/K+-ATPase and vacuolar type H+-ATPase protein abundance localization pointed out to activation of preexisting ATPases, non-bicarbonate pH buffering, or both, as the mechanism for endolymph pH-regulation. These results provide the first direct evidence showcasing the acid-base chemistry of the endolymph of OA-exposed fish favors otolith overgrowth, and suggests that this phenomenon will be more pronounced in species that count with more robust blood and endolymph pH regulatory mechanisms.

  • Pseudomonas aeruginosa β-carbonic anhydrase, psCA1, is required for calcium deposition and contributes to virulence

    2019, Cell Calcium

    Citation Excerpt :

    Due to their catalytic activity, CAs may drive the formation of CaCO3 under appropriate environmental conditions. The role of eukaryotic CAs in calcification has been shown in mollusks shells [41] and fish otoliths [42]. Membrane bound α-CA from coral Stylophora pistillata [43] and bovine CA [44] were shown to be involved in precipitation of CaCO3.

    Calcification of soft tissue leads to serious diseases and has been associated with bacterial chronic infections. However, the origin and the molecular mechanisms of calcification remain unclear. Here we hypothesized that a human pathogen Pseudomonas aeruginosa deposits extracellular calcium, a process requiring carbonic anhydrases (CAs). Transmission electron microscopy confirmed the formation of 0.1-0.2 μm deposits by P. aeruginosa PAO1 growing at 5 mM CaCl2, and X-ray elemental analysis confirmed they contain calcium. Quantitative analysis of deposited calcium showed that PAO1 deposits 0.35 and 0.75 mM calcium/mg protein when grown at 5 mM and 10 mM CaCl2, correspondingly. Fluorescent microscopy indicated that deposition initiates at the cell surface. We have previously characterized three PAO1 β-class CAs: psCA1, psCA2, and psCA3 that hydrate CO2 to HCO3, among which psCA1 showed the highest catalytic activity (Lotlikar et. al. 2013). According to immunoblot and RT-qPCR, growth at elevated calcium levels increases the expression of psCA1. Analyses of the deletion mutants lacking one, two or all three psCA genes, determined that psCA1 plays a major role in calcium deposition and contributes to the pathogen’s virulence. In-silico modeling of the PAO1 β-class CAs identified four amino acids that differ in psCA1 compared to psCA2, and psCA3 (T59, A61A, A101, and A108), and these differences may play a role in catalytic rate and thus calcium deposition. A series of inhibitors were tested against the recombinant psCA1, among which aminobenzene sulfonamide (ABS) and acetazolamide (AAZ), which inhibited psCA1 catalytic activity with KIs of 19 nM and 37 nM, correspondingly. The addition of ABS and AAZ to growing PAO1 reduced calcium deposition by 41 and 78, respectively. Hence, for the first time, we showed that the β-CA psCA1 in P. aeruginosa contributes to virulence likely by enabling calcium salt deposition, which can be partially controlled by inhibiting its catalytic activity.

  • Metabolic effects on carbon isotope biomarkers in fish

    2019, Ecological Indicators

    Citation Excerpt :

    Additionally, there has been variation in methods used to experimental derive M. For example, a range of different isotopic mixing models have been used (Jamieson et al., 2004; Kalish, 1991b; Solomon et al., 2006) and variation in values of carbon sources in calculations, with many studies using assumed rather than measured data (i.e. for DIC). Furthermore, environmental differences in experimentally-determined M have been found with freshwater fish possessing significantly lower proportions of metabolic carbon (∼17%) in otoliths than marine fish (Solomon et al., 2006; Tohse et al., 2004). M did not significantly increase with higher temperatures when tank was included in the statistical analyses.

    Carbon stable isotopes (δ13C) in animal tissues are a powerful tool for tracking biological and environmental change. However, carbon isotope signatures can be altered by both physiological and environmental factors which can cloud interpretation in their use as biomarkers. We investigated metabolic effects (by varying temperatures) on δ13C of three fish tissues (otolith, muscle and liver) and the proportional contributions of environmental water (dissolved inorganic carbon; DIC) and diet (metabolic sources). Juvenile Australasian snapper (Chrysophrys auratus) were laboratory-reared at four temperatures for up to two months and then δ13C in otolith, liver and muscle were measured using isotope-ratio mass spectrometry (IRMS). Temperature significantly altered δ13C signatures in all tissues. δ13C in otoliths reflected carbon signatures from diet and water DIC, with values and variation of proportional contributions influenced by temperature. In muscle and liver, we found differences in δ13C between tissues and across temperature treatments with concurrent high diet-to-tissue fractionation. We conclude that metabolic effects influenced carbon incorporation for all tissues, with otolith carbon providing valuable insights into field metabolic rates. However, metabolic effects complicated the use of soft-tissue to track diet. This study deepens our understanding of internal and external drivers of carbon isotopic signatures in fish tissues and enhances their utility as a biomarker in the field. Improved insight into biomarkers facilitates more accurate predictions of ecological and environmental change for better understanding and management of wild populations.

  • Molecular evolution of calcification genes in morphologically similar but phylogenetically unrelated scleractinian corals

    2014, Molecular Phylogenetics and Evolution

    Citation Excerpt :

    Orthologs of BMP were found to affect dorso-ventral axis formation in a scleractinian coral (Hayward et al., 2002), and shell formation in mollusks (Nederbragt et al., 2002). CAs have been shown to play important roles in the calcification of many invertebrates, e.g., mollusk shells (Gaume et al., 2011), as well as vertebrates, e.g., fish otoliths (Tohse et al., 2004). In corals, gene expression analyses found CAs to be expressed in post settlement polyps at the aboral disk (an area consistent with the onset of calcification), whereas in older polyps CAs were expressed in the septa (where calcification occurs through adulthood) (Grasso et al., 2008).

    Molecular phylogenies of scleractinian corals often fail to agree with traditional phylogenies derived from morphological characters. These discrepancies are generally attributed to non-homologous or morphologically plastic characters used in taxonomic descriptions. Consequently, morphological convergence of coral skeletons among phylogenetically unrelated groups is considered to be the major evolutionary process confounding molecular and morphological hypotheses. A strategy that may help identify cases of convergence and/or diversification in coral morphology is to compare phylogenies of existing “neutral” genetic markers used to estimate genealogic phylogenetic history with phylogenies generated from non-neutral genes involved in calcification (biomineralization). We tested the hypothesis that differences among calcification gene phylogenies with respect to the “neutral” trees may represent convergent or divergent functional strategies among calcification gene proteins that may correlate to aspects of coral skeletal morphology. Partial sequences of two nuclear genes previously determined to be involved in the calcification process in corals, “Cnidaria-III” membrane-bound/secreted α-carbonic anhydrase (CIII-MBSα-CA) and bone morphogenic protein (BMP) 2/4, were PCR-amplified, cloned and sequenced from 31 scleractinian coral species in 26 genera and 9 families. For comparison, “neutral” gene phylogenies were generated from sequences from two protein-coding “non-calcification” genes, one nuclear (β-tubulin) and one mitochondrial (cytochrome b), from the same individuals. Cloned CIII-MBSα-CA sequences were found to be non-neutral, and phylogenetic analyses revealed CIII-MBSα-CAs to exhibit a complex evolutionary history with clones distributed between at least 2 putative gene copies. However, for several coral taxa only one gene copy was recovered. With CIII-MBSα-CA, several recovered clades grouped taxa that differed from the “non-calcification” loci. In some cases, these taxa shared aspects of their skeletal morphology (i.e., convergence or diversification relative to the “non-calcification” loci), but in other cases they did not. For example, the “non-calcification” loci recovered Atlantic and Pacific mussids as separate evolutionary lineages, whereas with CIII-MBSα-CA, clones of two species of Atlantic mussids (Isophyllia sinuosa and Mycetophyllia sp.) and two species of Pacific mussids (Acanthastrea echinata and Lobophyllia hemprichii) were united in a distinct clade (except for one individual of Mycetophyllia). However, this clade also contained other taxa which were not unambiguously correlated with morphological features. BMP2/4 also contained clones that likely represent different gene copies. However, many of the sequences showed no significant deviation from neutrality, and reconstructed phylogenies were similar to the “non-calcification” tree topologies with a few exceptions. Although individual calcification genes are unlikely to precisely explain the diverse morphological features exhibited by scleractinian corals, this study demonstrates an approach for identifying cases where morphological taxonomy may have been misled by convergent and/or divergent molecular evolutionary processes in corals. Studies such as this may help illuminate our understanding of the likely complex evolution of genes involved in the calcification process, and enhance our knowledge of the natural history and biodiversity within this central ecological group.

  • Histochemical localisation of carbonic anhydrase in the inner ear of developing cichlid fish, Oreochromis mossambicus

    2008, Advances in Space Research

    Inner ear otolith growth in terms of mineralisation mainly depends on the enzyme carbonic anhydrase (CAH). CAH is located in specialised, mitochondria-rich macular cells (ionocytes), which are involved in the endolymphatic ion exchange, and the enzyme is responsible for the provision of the pH-value necessary for otolithic calcium carbonate deposition.

    In the present study, for the first time the localisation of histochemically demonstrated CAH was analysed during the early larval development of a teleost, the cichlid fish Oreochromis mossambicus.

    CAH-reactivity was observed already in stage 7 animals (onset of otocyst development; staging follows Anken et al. [Anken, R., Kappel, T., Slenzka, K., Rahmann, H. The early morphogenetic development of the cichlid fish, Oreochromis mossambicus (Perciformes, Teleostei). Zool. Anz. 231, 1–10, 1993]). Neuroblasts (from which sensory and supporting cells are derived) proved to be CAH-positive. Already at stage 12 (hatch), CAH-positive regions could be attributed to ionocyte containing regions both in the so-called meshwork and patches area of the macula (i.e., clearly before ionocytes can be identified on ultrastructural level or by employing immunocytochemistry).

    In contrast to the circumstances observed in mammalian species, sensory hair cells stained negative for CAH in the cichlid.

    With the onset of stage 16 (finray primordia in dorsal fin, yolk-sac being increasingly absorbed), CAH-reactivity was observed in the vestibular nerve. This indicates the onset of myelinisation and thus commencement of operation.

    The localisation of CAH in the inner ear of fish (especially the differences in comparison to mammals) is discussed on the basis of its role in otolith calcification.

    Since the vestibular system is a detector of acceleration and thus gravity, also aspects regarding effects of altered gravity on CAH and hence on the mineralisation of otoliths in an adaptive process are addressed.

  • Localization and diurnal variations of carbonic anhydrase mRNA expression in the inner ear of the rainbow trout Oncorhynchus mykiss

    2006, Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

    Citation Excerpt :

    The fact that the transport of protons, calcium and bicarbonate are all inhibited by acetazolamide (Mugiya et al., 1979; Payan et al., 1997; Tohse and Mugiya, 2001) indicates that CA has a central role in the transport of these ions via a reversible interconversion of bicarbonate, protons, and CO2 in this system. The present result, rtCAb mRNA expression in the transitional and squamous epithelia of the sacculus, is consistent with protein localization revealed by immunohistochemistry using anti-human CA II antibody (Mayer-Gostan et al., 1997; Tohse et al., 2004). On the other hand, the central area of the squamous epithelium induces small ionocytes, which may play important roles in ion transportation (Pisam et al., 1998).

    Physiological studies have suggested that carbonic anhydrase (CA) plays a central role in otolith biomineralization via ion transport. However, the presence and exact function of CA in the inner ear have not been determined. In the present study, to investigate the localization of CA and its involvement in otolith calcification, we cloned two cDNAs encoding CAs from the rainbow trout sacculus. These two cDNAs, designated rainbow trout CAa (rtCAa) and rtCAb, both had an open reading frame encoding 260 amino acids with a sequence identity of 78%. Remarkably, rtCAb has a high degree of homology (82%) with “high activity CA” in the zebrafish, and its mRNA expression showed variation in the range 1.9–11.4×104 copies/ng total RNA in the sacculus. In contrast, rtCAa mRNA was constantly expressed at approximately 3×104 copies/ng total RNA. In situ hybridization revealed that rtCAb mRNA was strongly expressed in the distal squamous epithelial cells and transitional epithelial cells, except the mitochondria-rich cells, whereas, rtCAa was localized in extrasaccular tissue. These results suggest that the rtCAb isozyme is involved in the daily increment formation and calcification of otoliths via phase and spatial differences of the bicarbonate supply to the endolymph.

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