A novel α-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2

EMBO Journal

Volumn 17, Issue 5, 1998, Pages 1208-1216

  Karlsson, Jan ^a   Ciarke, Adrian K ^a   Chen, Zhi Yuan ^b   Hugghins, Stephanie Y ^b   Park, Youn Il ^a   Husic, H David ^c   Moroney, James V ^b   Samuelsson, Göran ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c LAFAYETTE COLLEGE   (United States)

Author keywords

CCM; cia 3; Complementation; Thylakoid lumen; Transfer peptide

Indexed keywords

ANTIBODY; CARBON DIOXIDE; CARBONATE DEHYDRATASE; CHLOROPHYLL A; COMPLEMENTARY DNA; MEMBRANE ENZYME; THERMOLYSIN;

AMINO ACID SEQUENCE; ARTICLE; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; COSMID; ENZYME ACTIVITY; ENZYME LOCALIZATION; EUKARYOTE; FLUORESCENCE ANALYSIS; GENE SEQUENCE; GREEN ALGA; IMMUNOBLOTTING; MOLECULAR CLONING; NONHUMAN; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; SEQUENCE ANALYSIS; THYLAKOID MEMBRANE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CARBON DIOXIDE; CARBONIC ANHYDRASES; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GENETIC COMPLEMENTATION TEST; INTRACELLULAR MEMBRANES; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MUTATION; PHOTOSYNTHESIS; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; THERMOLYSIN;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EUKARYOTA;

EID: 0032473423     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.5.1208     Document Type: Article

References (52)

1. 2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Rev., 39, 215-233.
2. Allen,K.D. and Staehelin,L.A. (1994) Polypeptide composition, assembly and phosphorylation patterns of the photosystem II antenna system of Chlamydomonas reinhardtii. Planta, 194, 42-54.
3. Amoroso,G., Weber,C., Sultemeyer,D. and Fock,H. (1996) Intracellular carbonic anhydrase activities in Dunaliella tertiolecta (Butcher) and Chlamydomonas reinhardtii (Dangeard) in relation to inorganic carbon concentration during growth: further evidence for the existence of two distinct carbonic anhydrases associated with the chloroplasts. Planta, 199, 177-184.
4. Badger,M.R. and Price,G.D. (1994) The role of carbonic anhydrase in photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol., 45, 369-392.
5. Baker,N. and Bowyer,J. (1994) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. BIOS Scientific Publishers Ltd, Oxford, UK.
6. Bogsch,E., Brink,S. and Robinson,C. (1997) Pathway specificity for a ΔpH-dependent precursor thylakoid lumen protein is governed by a 'Sec-avoidance' motif in the transfer peptide and a 'Sec-incompatible' mature protein. EMBO J., 16, 3851-3859.
7. Brock,J.W., Hazell,L., Michl,D., Nielsen,V.S., Møller,B.L., Herrmann,R.G., Klösgen,R.B. and Robinson,C. (1993) Precursors of one integral and five lumenal thylakoid proteins are imported by isolated pea and barley thylakoids: optimisation of in vitro assays. Plant Mol. Biol., 23, 717-725.
8. 2. Plant Mol. Biol., 31, 443-448.
9. Chaddock,A.M., Mant,A., Karnauchov,I., Brink,S., Herrman,R.G., Klosgen,R.B. and Robinson,C. (1995) A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the ΔpH-dependent thylakoidal protein translocase. EMBO J., 14, 2715-2722.
10. 2 inducible gene encoding an alanine:α-ketoglutarate aminotransferase in Chlamydomonas reinhardtii. Plant Physiol., 112, 677-684.
11. 2-induced polypeptide in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 93, 12031-12034.
12. Frazén,L.-G., Rochaix,J.-D. and Heijne,G.v. (1990) Chloroplast transit peptides from the green alga Chlamydomonas reinhardtii share features with both mitochondrial and higher plant chloroplast presequences. FEBS Lett., 260, 165-168.
13. 2 concentration. Proc. Natl Acad. Sci. USA, 87, 4383-4387.
14. 2. Plant Physiol., 114, 237-244.
15. Genty,B., Briantais,J. and Baker,N. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta, 990, 87-92.
16. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust. J. Plant Physiol., 22, 131-160.
17. Hewett-Emmett,D. and Tashian,R.E. (1996) Functional diversity, conservation and convergence in the evolution of the α-, β- and γ- carbonic anhydrase gene families. Mol. Phys. Evol., 5, 50-77.
18. Husic,H.D. and Marcus,C.A. (1994) Identification of intracellular carbonic anhydrase in Chlamydomonas reinhardtii with a carbonic anhydrase-directed photoaffinity label. Plant Physiol., 105, 133-139.
19. Hutner,S.H., Provasoli,L., Schatz,A. and Haskins,C.P. (1950) Some approaches to the study of the role of metals in the metabolism of microorganisms. Proc. Am. Philos. Soc., 94, 152-170.
20. Johanningmeier,U. and Howell,S.H. (1984) Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii: possible involvement of chlorophyll synthesis precursors. J. Biol. Chem., 259, 13541-13549.
21. Karlsson,J., Hiltonen,T., Husic,H.D., Ramazanov,Z. and Samuelsson,G. (1995) Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol., 109, 533-539.
22. 2-dependent mutants of Chlamydomonas reinhardtii as studied by a new assay. Plant Physiol., 105, 1197-1202.
23. Khalifah,R. (1971) The carbon dioxide hydration activity of carbonic anhydrase, stop-flow kinetic studies on the native human isoenzymes B and C. J. Biol Chem., 246, 2561-2573.
24. Kindle,K.L. (1990) High frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 87, 1228-1232.
25. Komarova,Y., Doman,N. and Shaposhnikov,G. (1982) Two forms of carbonic anhydrase from bean chloroplasts. Biokhimiya, 47, 1027-1034.
26. Kulharni,R., Schaefer,M. and Golden,S. (1992) Transcriptional and posttranslational components of psbA response to high light intensity in Synechococcus sp. strain PCC 7942. J. Bacterial., 174, 3775-3781.
27. Laemmli,U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
28. Liljas,A., Hakansson,K., Jonsson,B.H. and Xue,Y. (1994) Inhibition and catalysis of carbonic anhydrase. Eur. J. Biochem., 219, 1-10.
29. Mason,C.B., Matthews,S., Bricker,T.M. and Moroney,J.V. (1991) A simplified procedure for the isolation of intact chloroplasts from Chlamydomonas reinhardtii. Plant Physiol., 97, 1576-1580.
30. Moroney,J.V. and Mason,C.B. (1991) The role of chloroplast in inorganic carbon acquisition by Chlamydomonas reinhardtii. Can. J. Bot., 69, 1017-1024.
31. Moroney,J.V., Husic,H.D. and Tolbert,N.E. (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol., 79, 177-183.
32. Moroney,J.V., Tolbert,N.E. and Sears,B.B. (1986) Complementation analysis of the inorganic carbon concentrating mechanism of Chlamydomonas reinhardtii. Mol. Gen. Genet., 204, 199-203.
33. Moubarak-Milad,A. and Stemler,A. (1994) Oxidation-reduction potential dependence of photosystem II carbonic anhydrase in maize thylakoids, Biochemistry, 33, 4432-1438.
34. Nielsen,V., Mant,A., Knoetzel,J., Møller,B. and Robinson,C. (1994) Import of barley photosystem I subunit N into the thylakoid lumen is mediated by a bipartite presequence lacking an intermediate processing site: role of the ΔpH in translocation across the thylakoid membrane. J. Biol. Chem., 269, 3762-3766.
35. 2 concentration mechanism: investigation by means of photosystem-deficient and carbonic anhydrase-deficient mutants of Chlamydomonas reinhardtii. Photosynthetica, 28, 131-140.
36. Pronina,N.A. and Semenenko,V.E. (1988) Localization of bound carbonic anhydrase in membranes of Chlorella cells. Sov. Plant Physiol., 35, 38-16.
37. 2 concentration in algae cells. In Baltscheffsky,M. (ed.), Current Research in Photosynthesis. Kluwer Academic Publishers, The Netherlands, Vol. IV, pp. 489-492.
38. Purton,S. and Rochaix,J.-D. (1994) Complementation of a Chlamydomonas reinhardtii mutant using a genomic cosmid library. Plant Mol. Biol., 24, 533-537.
39. 2-inducible 36-kilodalton protein is localized to the chloroplast envelope of Chlamydomonas reinhardtii. Plant Physiol., 101, 1195-1199.
40. 2 concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant, Cell Environ., 20, 147-154.
41. Rawat,M. and Moroney,J.V. (1991) Partial characterization of a new isoenzyme of carbonic anhydrase isolated from Chlamydomonas reinhardtii. J. Biol. Chem., 266, 9719-9723.
42. Robinson,C. and Mant,A. (1997) Targeting of proteins into and across the thylakoid membrane. Trends Plant Sci., 2, 431-437.
43. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Silflow,C.D., Chisholm,R.L., Conner,T.W. and Ranum,L.P.W. (1985) The two alpha tubulin genes of Chlamydomonas reinhardtii code for slightly different proteins. Mol. Cell. Biol., 5, 2389-2398.
45. Smith,R.G. (1988) Inorganic carbon transport in biological systems. Comp. Biochem. Physiol., 90, 639-654.
46. Spalding,M.H., Spreitzer,R.J. and Ogren,W.L. (1983) Carbonic anhydrase-deficient mutant of Chlamydomonas reinhardtii requires elevated carbon dioxide concentration for photoautotrophic growth. Plant Physiol., 73, 268-272.
47. Stemler,A. (1985) Carbonic anhydrase: molecular insights applied to photosystem II research in thylakoid membranes. In Berry,J. and Lucas,W. (eds), Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms. American Society of Plant Physiologists, Rockville, MD, pp. 377-387.
48. Stemler,A. and Jursinic,P. (1983) The effects of carbonic anhydrase inhibitors formate, bicarbonate acetazolamide, and imidazole on photosystem II in maize chloroplasts. Arch. Biochem. Biophys., 221, 227-237.
49. Sueoka,N. (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 46, 83-91.
50. Siiltemeyer,D., Amoroso,G. and Fock,H. (1995) Induction of intracellular carbonic anhydrases during the adaptation to low carbon concentrations in wild-type and ca-1 mutant cells of Chlamydomonas reinhardtii. Planta, 196, 217-224.
51. Tashian,R.E. (1989) The carbonic anhydrases: widening perspectives on their evolution, expression and function. BioEssays, 10, 186-192.
52. Warburg,O. and Krippahl,G. (1960) Notwendigkeit der kohlensaure für die chinon und ferricyanid-reaktionen in grünen grana. Z. Naturforsch., 15, 367-369.