Journal of Experimental Botany, Vol. 51, No. 348, pp. 1171-1178,
July 2000
© 2000 Oxford University Press
Review Article |
Primary sodium plasma membrane ATPases in salt-tolerant algae: facts and fictions
Julius-von-Sachs Institute of Bioscience, University of Würzburg, Julius-von-Sachs Platz 2, D-97082 Würzburg, Germany
Received 21 February 2000; Accepted 21 March 2000
Abstract
For thermodynamic reasons algae growing in media of both high salinity and high alkalinity require active export of sodium. However, experimental evidence for an active Na+-dependent cycle was scarce until recently, in contrast to the situation in marine bacteria (including cyanobacteria), fungi and animals. However, a review of literature reveals that some progress has been made in this respect, recently: data demonstrate that at least in two marine algae, Tetraselmis (Platymonas) viridis and Heterosigma akashiwo (syn. Olisthodiscus luteus), active Na+-export is carried out by means of a plasma membrane localized Na+-pump (apparent molecular mass 100–140 kDa). Biochemical characteristics of this vanadate-sensitive, but ouabain-resistant primary P-type Na+-ATPase are described and compared with the corresponding properties of Na+-ATPase from prokaryotes and animals. Alternative mechanisms for Na+-pumping are discussed.
Key words: Alkalinity, cytoplasmic pH, Dunaliella, Heterosigma, Na+-ATPase, membrane potential, Na+/H+-antiporter, plasma membrane, Platymonas, salinity, sodium pump, Tetraselmis.
Introduction
Active sodium export is a well-investigated phenomenon in bacteria (Skulachev, 1994
; Ivey et al., 1998, Horikoshi, 1998; Krulwich et al., 1998), fungi (Serrano et al., 1986; Haro et al., 1991; Ferrando et al., 1995; Marquez and Serrano, 1996; Benito et al., 1997; de Souza and Gomes, 1998) and animals (Glynn and Karlish, 1975; Stein, 1986). Whenever in a saline environment the passive Na+ flux into the cell (the apparent permeability coefficient PNa+ of the plasma membrane (PM) of marine phototrophs is in the order of 0.05–3x10-9 m s-1, Raven, 1976; Ritchie, 1992) increases the cytoplasmic Na+ concentration above a critical level, Na+ re-export into the environment is initiated (Na+ homeostasis). One obvious possibility of Na+ retranslocation is the coupling to inverse H+-gradients created by H+-ATPases. The well-known Na+/H+ antiporter (Padan and Schuldinger, 1993) utilizes these gradients by exchanging external H+ for internal Na+ (secondary energized Na+ export). When the proton motive force (pmf) 
µH+ is not large enough, because the membrane potential 
and/or the pH is too low, for example, because of alkaline external pH, primary active Na+ export mechanisms must take over, such as primary Na+ pumps (Ken-Dror et al., 1986; Stein, 1986; Benito et al., 1997) or Na+ motive NADH-ubiquinone oxidoreductase (Tokuda et al., 1985; Beattie et al., 1994; Pfenninger-Li et al., 1996). This review predominantly deals with the occurrence, properties and functions of Na+-ATPases in algae.
Reviewing the literature of the last ten years one gets the impression that only bacteria, cyanobacteria, fungi, and mammalia, but not algae or higher plants, possess Na+-ATPases in their plasma membranes (PM). This is surprising, since algae and halophytic higher plants also survive high salinity. In fact, algae such as Dunaliella species which can grow in the saturated salt solution in the Dead Sea. Marine algae, seaweeds, and sea grasses are exposed to NaCl concentration between 450 and 500 mM at pH values between 8 and 9. Similar salt concentrations can be measured in soil solution of salt-marshes inhabited by a large variety of herbaceous flowering plants. Likewise mangroves grow well despite transient flooding of their root system with sea water. Active Na+ extrusion has been postulated for a long time from in vivo studies with salt-tolerant algae (Balnokin and Medvedev, 1984; Weis and Pick, 1990; Katz et al., 1991, 1992; Pick, 1992; Balnokin, 1993). A discussion on blue-green algae (Ritchie, 1991,1992) also led to the postulation of a primary Na+ pump. The long research for the supposed plasma membrane Na+-ATPases (PMNA) in both marine algae and higher plant halophytes was initially unsuccessful, in spite of increasingly methodical progress in isolation, purification and characterization of bacterial, fungal and mammalian ATPases, and the powerful tools of immunobiology. One of the misleading assumptions during the screening was the supposed ouabain-sensitivity of the suggested Na+ pump, deduced from the ouabain sensitivity of the animal Na+/K+ -ATPase. Most attempts to demonstrate in vivo or in vitro any ouabain sensitivity of physiological reactions in salt-tolerant algae failed. Only later it was understood that ouabain sensitivity is caused by binding to a specific, regulatory amino acid domain of the Na+/K+-ATPase rather than to the catalytic site. If this sequence is missing in homologous enzymes, ouabain sensitivity will disappear without effect on the transport function.
Since screening remained unsuccessful for a long time, the question had to be raised whether algae have developed mechanisms to prevent internal salinization which are principally different from those existing in bacteria, fungi and animals. From the evolutionary point of view this seems to be rather unlikely. Alternatively, and more simple, it could be that the protocols developed for the isolation and purification of PM vesicles from marine and hypersaline algae were not appropriate and prevented the recognition and characterization of active Na+ pumps. This review summarizes recent progress made on the field of algal PMNA. It will demonstrate that, at least in the unicellular, non-vacuolated marine algae Tetraselmis viridis (Prasinophyceae) and Heterosigma akashiwo (Cryptophyta) a PMNA is involved in the Na+ cycle. Surprisingly, with the same techniques as applied to these two algae, a PMNA has not been detected so far in the extremely salt-tolerant, non-vacuolated alga Dunaliella salina (Chlorophyta). It is obvious that current knowledge about its properties lags far behind of that what is known about bacterial, cyanobacterial, fungal, and mammalian Na+-pumps. The reason for this will be discussed and future perspectives described.
Low µH+ at high alkalinity and salinity: a thermodynamical approach
Unicellular marine and hypersaline algae such as Tetraselmis viridis and Dunaliella salina (syn. D. parva) are able to grow simultaneously at NaCl concentrations between 0.3 and 3 M and a pH range between 8 and 10 (Pick, 1992; Balnokin et al., 1997; Gimmler and Degenhardt, 2000). As in all other algae, both species possess H+ ATPase (Gimmler et al., 1989b; Pick, 1992; Balnokin and Popova, 1994) and Na+/H+ antiporters in their PM (Katz et al., 1986, 1989, 1992; Pick, 1992; Popova and Balnokin, 1992) (Fig. 1). At the alkaline external pH value of 9.0 the cytoplasmic pH of Tetraselmis is close to 7.6 (Balnokin et al., 1997) and that of Dunaliella close to 7.3 (Gimmler et al., 1988). The cytoplasmic Na+ concentration of Tetraselmis is about 26 mM (at sea water salinity), whereas that of Dunaliella is difficult to assess precisely at molar external concentrations (Pick, 1992). For convenience, an average value of 200 mM is used for this alga for the calculations of Fig. 1. From the data of Fig. 1 and equations which describe the activities of a Na+/H+ antiporter,
 |
 | (1) |
 | (2) |
, R, T, F, and n are the usual thermodynamic parameters). Calculated numbers in Fig. 1 should be taken as rough approximations rather than as exact figures.
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For Tetraselmis viridis the external H+concentration required to drive an electroneutral antiporter varies between 0.4 and 0.8 µM H+ (Fig. 1
), corresponding to pH values between 6.1 and 6.4. In the case of an electrogenic antiporter with a H+/Na+ stoichiometry n=2 or 3, membrane potentials between -243 and -160 mV would be required. Membrane potentials of Tetraselmis cells have not been determined experimentally, but, in general, membrane potentials (
co) of marine algae do not exceed -100 mV. In the work of Raven (Raven, 1976) values of -70 mV are quoted for Bryopsis plumosa, -72 to -75 mM for Chaetomorpha darwinii, - 80 mV for Halocystis ovalis, -42 mV for Porphyra perforata, and -71 mV for Valonia ventricosa. Only for Acetabularia mediterranea a relatively high value of -180 mV was recorded. For Dunaliella parva the required external H+ concentration to drive an electroneutral antiporter varies between 0.4 and 0.8 µM H+ (Fig. 1), corresponding to pH values between 6.1 and 6.4. In the case of an electrogenic antiporter with a H+/Na+ stoichiometry n=2 or 3, membrane potentials between -260 and -180 mV would be required to maintain the experimentally determined cytoplasmic Na+ concentrations. However, experimentally determined membrane potentials of Dunaliella vary between -50 and -100 mV (Gimmler et al., 1989a; Remis et al., 1992). Since all available data on the PM localized Na+/H+ antiporters of Dunaliella (Katz et al., 1986, 1989, 1991, 1992; Pick, 1992) and Tetraselmis (Popova and Balnokin, 1992) imply an electroneutral transport, the conclusion can be drawn from data of Fig. 1, that above an external pH of 8 and at elevated external Na+ concentrations, the Na+/H+ antiporter (may it be electrogenic or electroneutral) is not sufficient to sustain Na+ homeostasis of these algae. Some other mechanism or mechanisms are responsible for the export of Na+.
The available data do not exclude the possibility that at neutral or slightly acid pH values a perfect Na+ cycle could be performed by a Na+/H+ antiporter. Thus the Na+/H+ antiporter and the additional Na+ exporting mechanism required for alkaline conditions may be complementary and enable algae to survive in saline environments within a broad range of H+ concentrations. Also in some bacteria the Na+/H+ antiporter as a sodium extrusion system has been suggested to play a supplementary role to the Na+-ATPase, particular at acidic to neutral external pH values (Kawano et al., 1998). Similar conclusions have been drawn from in vivo studies with Dunaliella cells (Katz et al., 1991; Pick, 1992): the most important function of the Na+/H+ antiporter was suggested to be the regulation of the internal pH rather than Na+ homeostasis. However, the question arises in such a case, why should a Na+/H+ antiporter be more useful in pH homeostasis than in the regulation of active H+-export and/or passive H+-uniport.
Furthermore, data of Fig. 1 do not permit any conclusion about the required mechanism of active Na+ export. However, research was initiated to demonstrate, at least for marine algae cultured at alkaline pH values, (a) the existence of a Na+-dependent ATP hydrolysis in plasma membranes and (b) ATP-dependent Na+ transport. Finally (c) an enzyme catalysing (a) and (b) has to be isolated and characterized.
Na+dependent ATP-hydrolysis
PM vesicles of Tetraselmis viridis and Heterosigma akashiwo catalyse a Mg2+ dependent ATP-hydrolysis stimulated by Na+ (Wada et al., 1989; Shono et al., 1995; Balnokin et al., 1997). ATP-hydrolysis is maximal at pH values between 8 and 9, it is inhibited by vanadate, but not inhibited by ouabain. The Km values for ATP is 0.88 mM and that for Na+ 12 mM (Shono et al., 1995). No such data have been reported for Dunaliella. However, it is striking that in contrast to the pH profile of vanadate-sensitive ATP hydrolysis of PM vesicles isolated from Dunaliella acidophila, which exhibits a peak at pH 6, the saline Dunaliella species exhibit either a broad optimal range between pH 6 and 9 (Gimmler et al., 1989b; Weiss et al., 1991; Pick, 1992) or a narrow peak at pH 8.5 (Smahel et al., 1990) (Fig. 2). These data might indicate the overlapping of ATP-hydrolysis catalysed by two distinct ATPases. At a pH of 7.6, vanadate-sensitive ATP hydrolysis of Dunaliella parva PM vesicles is slightly, but significantly, stimulated by Na+ and activity is higher in the presence of permeant anions (2 et al., 1989b).
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ATP-dependent Na+transport
PM vesicles of Tetraselmis viridis and Heterosigma akashiwo also catalyse ATP dependent Na+-uptake, measured as uptake of 22Na+ (Balnokin and Popova, 1994; Shono et al., 1996; Balnokin et al., 1997). Substrate kinetics of the enzyme reconstituted into liposomes are very similar to that of Na+-dependent ATP-hydrolysis (Fig. 3A, B; Shono et al., 1996) and the pH profile of transport can be distinguished from that of H+-transport by its alkaline optimum (Fig. 4; Balnokin et al., 1997). The vanadate-sensitive Na+ transport is not inhibited by uncouplers like CCCP, FCCP or monensin, which indicates that the transport does not require pH as a driving force. It is also not inhibited by amiloride, which blocks the Na+/H+ antiporter activity. ATP- dependent, uncoupler-resistant Na+ uptake was observed only in the presence of permeant anions such as chloride and nitrate, indicating an electrogenic translocation. No corresponding data have been published for Dunaliella. However, transport experiments with PM vesicles isolated from marine Dunaliella species seem to be more difficult than with vesicles from other algae. Not even ATP-dependent and vanadate-sensitive H+ transport catalysed by the PM H+-ATPase has been demonstrated in most studies (Weis et al., 1989; Gimmler et al., 1989b; Smahel et al., 1990; Pick, 1992). This may indicate leakiness of the vesicle membrane. It is worthwhile to mention that the methods selected to isolate PM vesicles from Tetraselmis and Heterosigma were much more sophisticated than those applied to Dunaliella and resulted in a much purer PM fraction as judged from contamination of the PM fraction by thylakoid membranes (chlorophyll as marker). For Heterosigma a method was applied in which PM was bound to positively charged micro beads; from the micro bead-bound PM fraction Na+-ATPase was isolated and reconstituted into liposomes. For the isolation of PM vesicles from Tetraselmis the mild method of Balnokin et al. (Balnokin et al., 1993) was used, which is characterized by avoiding total mechanical or osmotic rupture of cells. Instead, cells were partially lysed enzymically in the presence of glycerol and ATP; then under the influence of a very small hypoosmotic shock, PM vesicles formed exclusively at the apical (flagellar) pole of the cell. By using this method contamination with other cellular membranes is extremely low, but unfortunately the yield was also very low. It is assumed that more attempts are required to obtain improved quality of PM preparations from Dunaliella cells, particular in respect to native ion permeability.
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Molecular properties of the Na+-ATPase of Tetraselmis and Heterosigma
The molecular mass of the supposed Na+-ATPase as revealed from unidimensional SDS-PAGE was 100 kDa (Tetraselmis, Popova et al., 1998, 1999) and 140 kDa, respectively (Heterosigma, Wada et al., 1992). In Heterosigma the enzyme exhibited an epitope at the amino-terminal region identical to that known for the mammalian Na+/K+-ATPase (Wada et al., 1992). Extended immunobiological studies with Tetraselmis PM vesicles and antibodies raised against animal Na+/K+-ATPase have not been carried out. Corresponding studies with PM vesicles isolated from Dunaliella salina and antibodies against various subunits and domains of P-types of ATPase (U Pick, M Weiss and H Gimmler, unpublished results) did not yield the expected evidence in favour of a Na+-ATPase, although a large number of various antibodies were tested: for example, antibodies against the 
-subunit and the ß-subunit and the holoenzyme of animal Na,K-ATPase (Research Diagnostics and raised by S Karlish, Israel). Furthermore, an antibody raised against an unknown P-type ATPase (definitely different from the H+-ATPase and Ca2+-ATPase) isolated from the PM of Dunaliella salina by Pick (Israel) was tested. Some cross-reactions of PM proteins from Dunaliella salina with antibodies against both subunits of the animal Na,K-ATPase and the P-type ATPase of Dunaliella salina mentioned above were observed, but no clear cut specificity and no agreement with known molecular weights of the enzymes could be detected so far. This is a severe set-back, since in contrast to the measurement of transport reactions, binding of antibodies does not depend on the native ion permeability of the membranes. Thus it is fair to state that, at present, the results of immunological studies with PM vesicles of Dunaliella can be taken neither as an argument for the existence of a primary Na+ pump nor against it.
The Na+-ATPase of Tetraselmis and Heterosigma belongs to the family of P-type ATPases
Phosphorylation studies applying 
-32P-ATP showed that, as for the animal Na+/K+-ATPase a Na+-dependent phosphorylation takes place during the catalytic cycle of the enzyme during the uptake of Na+ into PM vesicles of Tetraselmis and Heterosigma (Wada et al., 1989; Shono et al., 1995; Popova et al., 1998, 1999). The phosphorylation of the 100 kDa (140 kDa) intermediate is inhibited by vanadate, ADP and KCl, but is not affected by the inhibitor of protein kinases, stauroporin. Hydroxylamine caused cleavage of 32P, indicating the involvement of acyl-phosphate linkages. The Km of the phosphorylation reaction for Na+ varied between 5 and 12 mM (Fig. 3). Protein phosphorylation of the 100 kDa protein was more pronounced at alkaline pH than at slightly acid to neutral pH (Fig. 4). Results of pulse-chase experiments indicated a rapid turnover of phosphorylation, which is accelerated by high concentrations of ATP and Mg2+. Data agree with the view that in the PM of the marine algae Heterosigma and Tetraselmis an electrogenic Na+-ATPase exists which has the properties of a P-, (E1E2) type of ATPase (Popova et al., 1998, 1999) according to the Albers-Post scheme (Stein, 1986). However, there is no evidence so far that the enzyme exchanges sodium against potassium as the animal Na+/K+-ATPase. Under alkaline conditions Dunaliella salina PM vesicles phosphorylated proteins with the apparent molecular masses 145 kDa (main band) and 90, 56, and 20 kDa (minor bands) (U Pick, M Weiss, H Gimmler, unpublished results). The major band was in the range of molecular masses of P-type ATPases. Preliminary tests indicated a Na+ dependence of the phosphorylation of this protein, but results have to be confirmed. The apparent molecular weight of 145 kDa of this phosphoprotein unfortunately overlaps in size with a 150 kDa protein of the PM of Dunaliella salina (Fisher et al., 1997, 1998) which is based on its cDNA-deduced sequence belongs presumably to the transferrin family. Interestingly, the amount of this 150 kDa protein increased not only upon iron deficiency (as would be expected from a transferrin) but also with rising salinity (as could be postulated from a Na+-pump). At present nothing is known about phosphorylation of transferrins. In the future more attention should be paid to the analysis whether or not a single or two entirely different proteins is/are being investigated.
Do data permit generalization for algae?
Summarizing, the evidence for the existence of a P-type Na+-ATPase in the PM of Tetraselmis and Heterosigma is strong. However, at present it is not permitted to generalize results obtained from only two algae to all the algae, especially since all efforts to demonstrate a PMNA in the extremely salt-tolerant Dunaliella have failed so far. The latter alga is a very well investigated important model system in algal stress physiology (Pick, 1992, 1998). Before final conclusions can be drawn, more algae of different taxonomic origins, thriving well at alkaline pH and high salinity should be studied. It should be kept in mind (1) that algae are known to be a polyphyletic grouping of organisms distinguished by primary or secondary endosymbioses which permit them to be photosynthesized and (2) that within bacteria different mechanisms of Na+ export have been shown, depending on the adaptation of species to alkalinity and salinity.
Alternatives for Na+-ATPases in the algal plasma membrane?
The PM of several marine bacteria and cyanobacteria has been shown to contain various redox systems involved in the active export of sodium, e.g. a Na+ transport NADH:quinone reductase (Tokuda and Unemoto, 1981, 1984; Tokuda et al., 1985; Hayashi and Unemoto, 1987; Unemoto and Hayashi, 1993; Pfenninger-Li et al., 1996) or a Na+ transporting cytochrome oxidase (Park et al., 1996). However, different from prokaryotes, the PM of algae is not a coupling membrane containing a complete respiratory chain or photosynthetic electron transport chain. Nevertheless, it was recently demonstrated, that the algal PM may also contain some residual redox chains (Nespurkova et al., 1993; Berger and Brownlee, 1994; Moog and Brüggemann, 1994; Lynnes and Weger, 1996; Chen et al., 1996a, b; Vanden-Driessche et al., 1997) which, theoretically, may serve in Na+ pumping. At present, they are biochemically much less well characterized than their bacterial counterparts. Their function is assigned so far to anion pumping (electron-anion antiport, Nespurkova et al., 1993), reduction of extracellular iron (Moog and Brüggemann, 1994; Chen et al., 1996b), or uptake of K+ (Chen et al., 1996b). Of particular interest with respect to the so far unsuccessful demonstration of a Na+-ATPase in the PM of the extremely salt-tolerant alga Dunaliella is the observation that the PM of this alga contains at least residual redox chains (Chen et al. 1996a, b).
Conclusions and further research
Data summarized in this review indicate that the marine algae Tetraselmis viridis and Heterosigma akashiwo possess an electrogenic, vanadate-sensitive, ouabain-resistant PM localized Na+-ATPase. It is unclear as yet, whether an exchange against K+ is involved as with the animal Na,K-ATPase. Data also suggest a flexible coupling of the sodium cycle in salt-tolerant algae as it has been observed for salt-tolerant prokaryotes: at acid to neutral pH the secondary energized Na+/H+-antiporter exports sodium in exchange against H+, whereas at alkaline pH the Na+-ATPase takes over. However, it is still an open question which factors regulate the functioning of these two Na+ exporting systems. In future, it has to be shown whether all algae thriving in saline environments at alkaline pH possess a primary sodium pump. Theoretically, algal species from hypersaline environments such as Dunaliella should require such pumps even more urgently than marine algae. It is also worthwhile elaborating as to whether non-marine species of different taxonomic origin are able to express a PMNA. For a rapid screening, immunobiological techniques should be applied more than has been done until now.
After elucidation of the Na+ cycle in non-vacuolated marine algae, vacuolated species should also be investigated, because in these algae transport across the tonoplast may be involved in Na+ homeostasis. Such investigations would lead to the study of higher plant halophytes, which in nature often encounter high salinity and alkaline pH values at the same time. In fact, the first evidence for an outward directed, ouabain-sensitive sodium pump in excised barley roots was presented almost 30 years ago (Nassery and Baker, 1972). These results do not seem to have been followed up by other workers. Modern reviews on roots of higher plants take into account for pH homeostasis only the presence of H+-ATPases in the plasma membrane and the tonoplast and a tonoplast Na+/H+-antiporter (Rausch et al., 1996). However, at the end of the reviews, the authors come to the conclusion that ‘not a single plant has as yet been studied in sufficient detail to allow a comprehensive evaluation of the relative importance of individual transport processes for the salt tolerance of an intact plant’. Nevertheless, also the need of ions other than H+ to allow an H+-ATPase in the plasma membrane to act in the regulation of cytoplasmic pH rather than generating just a very large inside negative electrical potential difference (co) in roots must be considered (Marschner, 1995). Since salinity is a world-wide agricultural problem, the search for mechanisms of active sodium extrusion in root cells has to continue. Experimental strategies will be the same as for algae, particular as for vacuolated algae. A prerequisite will be an advanced protocol for the isolation of rhizodermal protoplasts and rhizodermal PM vesicles.
Acknowledgments
This study was supported by the Deutsche Forschungsgemeinschaft (SFB 251, TP A2).
Notes
1 Fax: +49 0931 888 6158. E-mail: gimmler{at}botanik.uni\|[hyphen]\|wuerzburg.de 
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