Primary structure and effect of pH on the expression of the plasma membrane H(+)-ATPase from Dunaliella acidophila and Dunaliella salina. (2024)

PMCID: PMC158103

M Weiss and U Pick

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Abstract

The plasma membrane H(+)-ATPase gene was cloned and sequenced from the extremely acidophilic green alga Dunaliella acidophila and from the extremely halotolerant Dunaliella salina. A special feature of the Dunaliella H(+)-ATPase is an extended C-terminal domain. The deduced amino acid sequences of the two proteins are 75% identical but differ in their C terminus. A hydrophilic loop within this domain in D. salina, which presumably faces the cell exterior, has a high ratio of acidic over basic amino acids, typical of halophilic proteins. The amount of the ATPase protein in plasma membranes and the level of its mRNA transcript in D. acidophila are far higher than in D. salina, suggesting that D. acidophila overexpresses the enzyme. A pH shift from 9.0 to 7.0 induces in D. salina a large increase in the level of the H(+)-ATPase mRNA and in the amount of the H(+)-ATPase protein. This suggests that the expression of the H(+)-ATPase in D. salina is pH-regulated at the transcriptional level. The implications of these findings are discussed with respect to the adaptive pressures imposed on these algal species by their exceptional environmental conditions.

• Ben-Amotz A, Avron M. The Role of Glycerol in the Osmotic Regulation of the Halophilic Alga Dunaliella parva. Plant Physiol. 1973 May;51(5):875–878. [PMC free article] [PubMed] [Google Scholar]
• Church GM, Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. [PMC free article] [PubMed] [Google Scholar]
• Dym O, Mevarech M, Sussman JL. Structural features that stabilize halophilic malate dehydrogenase from an archaebacterium. Science. 1995 Mar 3;267(5202):1344–1346. [PubMed] [Google Scholar]
• Ewing NN, Wimmers LE, Meyer DJ, Chetelat RT, Bennett AB. Molecular Cloning of Tomato Plasma Membrane H-ATPase. Plant Physiol. 1990 Dec;94(4):1874–1881. [PMC free article] [PubMed] [Google Scholar]
• Fisher M, Gokhman I, Pick U, Zamir A. A salt-resistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem. 1996 Jul 26;271(30):17718–17723. [PubMed] [Google Scholar]
• Fisher M, Pick U, Zamir A. A Salt-Induced 60-Kilodalton Plasma Membrane Protein Plays a Potential Role in the Extreme Halotolerance of the Alga Dunaliella. Plant Physiol. 1994 Dec;106(4):1359–1365. [PMC free article] [PubMed] [Google Scholar]
• Frolow F, Harel M, Sussman JL, Mevarech M, Shoham M. Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe-2S ferredoxin. Nat Struct Biol. 1996 May;3(5):452–458. [PubMed] [Google Scholar]
• Hager KM, Mandala SM, Davenport JW, Speicher DW, Benz EJ, Jr, Slayman CW. Amino acid sequence of the plasma membrane ATPase of Neurospora crassa: deduction from genomic and cDNA sequences. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7693–7697. [PMC free article] [PubMed] [Google Scholar]
• Harper JF, Surowy TK, Sussman MR. Molecular cloning and sequence of cDNA encoding the plasma membrane proton pump (H+-ATPase) of Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1234–1238. [PMC free article] [PubMed] [Google Scholar]
• Hopp TP, Woods KR. Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3824–3828. [PMC free article] [PubMed] [Google Scholar]
• Katz A, Bental M, Degani H, Avron M. In Vivo pH Regulation by a Na/H Antiporter in the Halotolerant Alga Dunaliella salina. Plant Physiol. 1991 May;96(1):110–115. [PMC free article] [PubMed] [Google Scholar]
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed] [Google Scholar]
• Palmgren MG, Christensen G. Functional comparisons between plant plasma membrane H(+)-ATPase isoforms expressed in yeast. J Biol Chem. 1994 Jan 28;269(4):3027–3033. [PubMed] [Google Scholar]
• Popova LG, Balnokin YV. H(+)-translocating ATPase and Na+/H+ antiport activities in the plasma membrane of the marine alga Platymonas viridis. FEBS Lett. 1992 Sep 14;309(3):333–336. [PubMed] [Google Scholar]
• Sekler I, Gläser HU, Pick U. Characterization of a plasma membrane H(+)-ATPase from the extremely acidophilic alga Dunaliella acidophila. J Membr Biol. 1991 Apr;121(1):51–57. [PubMed] [Google Scholar]
• Sekler I, Pick U. Purification and Properties of a Plasma Membrane H+-ATPase from the Extremely Acidophilic Alga Dunaliella acidophila. Plant Physiol. 1993 Mar;101(3):1055–1061. [PMC free article] [PubMed] [Google Scholar]
• Sekler I, Remis D, Gimmler H, Pick U. Inhibition of the plasma-membrane H(+)-ATPase from Dunaliella adidophila by omeprazole. Biochim Biophys Acta. 1993 Apr 5;1142(1-2):88–92. [PubMed] [Google Scholar]
• Sekler I, Weiss M, Pick U. Activation of the Dunaliella acidophila plasma membrane H(+)-ATPase by trypsin cleavage of a fragment that contains a phosphorylation site. Plant Physiol. 1994 Aug;105(4):1125–1132. [PMC free article] [PubMed] [Google Scholar]
• Serrano R, Kielland-Brandt MC, Fink GR. Yeast plasma membrane ATPase is essential for growth and has hom*ology with (Na+ + K+), K+- and Ca2+-ATPases. Nature. 1986 Feb 20;319(6055):689–693. [PubMed] [Google Scholar]
• Serrano R, Portillo F, Monk BC, Palmgren MG. The regulatory domain of fungal and plant plasma membrane H(+)-ATPase. Acta Physiol Scand Suppl. 1992;607:131–136. [PubMed] [Google Scholar]
• Vara F, Serrano R. Partial purification and properties of the proton-translocating ATPase of plant plasma membranes. J Biol Chem. 1982 Nov 10;257(21):12826–12830. [PubMed] [Google Scholar]
• Wolf AH, Slayman CW, Gradmann D. Primary structure of the plasma membrane H(+)-ATPase from the halotolerant alga Dunaliella bioculata. Plant Mol Biol. 1995 Jul;28(4):657–666. [PubMed] [Google Scholar]