1887

Abstract

Intact cells of the purple non-sulfur bacterium growing anaerobically, but not aerobically, contain carbonic anhydrase (CA) activity. The native enzyme was purified >2000-fold to apparent homogeneity and found to be a dimer with an estimated molecular mass of 54 kDa and a subunit molecular mass of 27 kDa. The CA gene () was cloned and its sequence revealed that it was homologous to α-type CAs. The upstream region of was fused to the gene and β-galactosidase activity was measured under different growth conditions. Acetazolamide inhibited purified CA with an IC in the range of 10 M, and in the culture media concentrations as low as 30 μM inhibited phototrophic growth under anaerobic, light conditions when bicarbonate was used. An :: mutant strain was constructed by insertion of a kanamycin-resistance cassette and showed a growth pattern similar to wild-type cells grown in the presence of CA inhibitor. CO gas supplied as an inorganic carbon source reversed the effect of mutation or acetazolamide. CA activity measurements, fusion and Western blot experiments confirmed that CA is expressed under different anaerobic conditions independently of bicarbonate or CO and that there is no expression under aerobic conditions.

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2000-11-01
2019-10-23
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References

  1. Alber, B. E. & Ferry, J. G. ( 1994; ). A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci USA 91, 6909-6913.[CrossRef]
    [Google Scholar]
  2. Armstrong, J. M., Myers, D. V., Verpoorte, J. A. & Edsall, J. T. ( 1966; ). Purification and properties of human erythrocyte carbonic anhydrases. J Biol Chem 21, 5137-5149.
    [Google Scholar]
  3. Badger, M. R. & Price, G. D. ( 1992; ). The CO2 concentrating mechanism in cyanobacteria and green algae. Physiol Plant 84, 606-615.[CrossRef]
    [Google Scholar]
  4. Blake, M. S., Johnston, K. H., Russel-Jones, G. J. & Gotschild, E. C. ( 1984; ). A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem 136, 175-179.[CrossRef]
    [Google Scholar]
  5. Bradford, M. M. ( 1976; ). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.[CrossRef]
    [Google Scholar]
  6. Brandner, J. P., McEwan, A. G., Kaplan, S. & Donohue, T. J. ( 1989; ). Expression of the Rhodobacter sphaeroides cytochrome c2 structural gene. J Bacteriol 171, 360-368.
    [Google Scholar]
  7. Braus-Stromeyer, S. A., Schnappauf, G., Braus, G. H., Gossner, A. S. & Drake, H. L. ( 1997; ). Carbonic anhydrase in Acetobacterium woodii and other acetogenic bacteria. J Bacteriol 179, 7197-7200.
    [Google Scholar]
  8. Brenner, V., Inui, M., Nunoura, N., Momma, K. & Yukawa, H. ( 1998; ). Studies on CO2 fixation in PNSB: utilization of waste as the additional source of carbon for CO2 fixation by PNSB. In Advances in Chemical Conversions for Mitigating Carbon Dioxide: Studies in Surface Science and Catalysis, vol. 114, pp. 593-596. Edited by T. Inui, M. Anpo, K. Izui, S. Yanagida & T. Yamaguchi. Amsterdam: Elsevier.
  9. Buchanan, B. B., Evans, M. C. W. & Arnon, D. I. ( 1967; ). Ferredoxin-dependent carbon assimilation in Rhodospirillum rubrum. Arch Mikrobiol 59, 32-40.[CrossRef]
    [Google Scholar]
  10. Burnell, J. N., Gibbs, M. J. & Hatch, M. D. ( 1990; ). Spinach chloroplastic carbonic anhydrase: nucleotide sequence analysis of cDNA. Plant Physiol 92, 37-40.[CrossRef]
    [Google Scholar]
  11. Chirica, L. C., Elleby, B., Jonsson, B.-H. & Lindskog, S. ( 1997; ). The complete sequence, expression in Escherichia coli, purification and some properties of carbonic anhydrase from Neisseria gonorrhoeae. Eur J Biochem 244, 755-760.[CrossRef]
    [Google Scholar]
  12. Coleman, J. R., Berry, J. A., Togasaki, R. K. & Grossman, A. R. ( 1984; ). Identification of extracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 76, 472-477.[CrossRef]
    [Google Scholar]
  13. Du, S., Bird, T. H. & Bauer, C. E. ( 1998; ). DNA binding characteristics of RegA. J Biol Chem 273, 18509-18513.[CrossRef]
    [Google Scholar]
  14. Eriksson, A. E., Jones, T. A. & Liljas, T. A. ( 1988; ). Refined structure of human carbonic anhydrase II at 2 Å resolution: proteins. Struct Funct Genet 4, 274-282.[CrossRef]
    [Google Scholar]
  15. Ferguson, K. A. ( 1964; ). Starch-gel electrophoresis – application to the classification of pituitary proteins and polypeptides. Metabolism 13, 985-1002.[CrossRef]
    [Google Scholar]
  16. Fujii, T., Nakazawa, A., Sumi, N., Tani, H., Ando, A. & Yabuki, M. ( 1983; ). Utilization of alcohols by Rhodopseudomonas sp. No. 7 isolated from n-propanol-enrichment cultures. Agric Biol Chem 47, 2747-2753.[CrossRef]
    [Google Scholar]
  17. Fukuzawa, H., Suzuki, E., Komukai, Y. & Miyachi, S. ( 1992; ). A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Proc Natl Acad Sci USA 89, 4437-4441.[CrossRef]
    [Google Scholar]
  18. Gill, S. R., Fedorka-Cray, P. J., Tweten, R. K. & Sleeper, B. P. ( 1984; ). Purification and properties of the carbonic anhydrase of Rhodospirillum rubrum. Arch Microbiol 138, 113-118.[CrossRef]
    [Google Scholar]
  19. Guilloton, M. B., Korte, J. J., Lamblin, A. F., Fuchs, J. A. & Anderson, P. M. ( 1992; ). Carbonic anhydrase in Escherichia coli. J Biol Chem 267, 3731-3734.
    [Google Scholar]
  20. Harwood, C. S. & Gibson, J. ( 1988; ). Anaerobic and aerobic metabolism of diverse aromatic compounds by the photosynthetic bacterium Rhodopseudomonas palustris. Appl Environ Microbiol 54, 712-717.
    [Google Scholar]
  21. Hatch, M. D. & Burnell, J. N. ( 1990; ). Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. Plant Physiol 93, 380-383.
    [Google Scholar]
  22. von Heijne, G. ( 1984; ). How signal sequences maintain cleavage specificity. J Mol Biol 173, 243-251.[CrossRef]
    [Google Scholar]
  23. Hewett-Emmett, D. & Tashian, R. E. ( 1996; ). Functional diversity, conservation, and convergence in the evolution of the α, β, γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5, 50-77.[CrossRef]
    [Google Scholar]
  24. Imhoff, J. F. ( 1995; ). Taxonomy and physiology of photosynthetic purple bacteria and green sulfur bacteria. In Anoxygenic Photosynthetic Bacteria: Advances in Photosynthesis, pp. 1-15. Edited by R. E. Blankenship, M. T. Madigan & C. E. Bauer. Dordrecht: Kluwer.
  25. Inui, M., Dumay, V., Zahn, K., Yamagata, H. & Yukawa, H. ( 1997; ). Structural and functional analysis of the phosphoenolpyruvate carboxylase gene of Rhodopseudomonas palustris No. 7. J Bacteriol 179, 4942-4945.
    [Google Scholar]
  26. Inui, M., Nakata, K., Roh, J. H., Zahn, K. & Yukawa, H. ( 1999; ). Molecular and functional characterization of the Rhodopseudomonas palustris No. 7 phosphoenolpyruvate carboxykinase gene. J Bacteriol 181, 2689-2696.
    [Google Scholar]
  27. Inui, M., Roh, J. H., Zahn, K. & Yukawa, H. ( 2000; ). Structural analysis of the cryptic plasmid pMG101 from Rhodopseudomonas palustris and construction of stable cloning vectors. Appl Environ Microbiol 66, 54-63.[CrossRef]
    [Google Scholar]
  28. Joshi, H. M. & Tabita, F. R. ( 1996; ). A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc Natl Acad Sci USA 93, 14515-14520.[CrossRef]
    [Google Scholar]
  29. Kaplan, A., Schwarz, R., Lieman-Hurwitz, J. & Reinhold, L. ( 1991; ). Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol 97, 851-855.[CrossRef]
    [Google Scholar]
  30. Karlsson, J., Clarke, A. K., Chen, Z-Y., Hugghins, S. Y., Park, Y.-I., Husic, H. D., Moroney, J. V. & Samuelsson, G. ( 1998; ). A novel α-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17, 1208-1216.[CrossRef]
    [Google Scholar]
  31. Kimpel, D. L., Togasaki, R. K. & Miyachi, S. ( 1983; ). Carbonic anhydrase in Chlamydomonas reinhardtii. I. Localization. Plant Cell Physiol 24, 255-259.[CrossRef]
    [Google Scholar]
  32. Lindskog, S., Henderson, L. E., Kannan, K. K., Liljas, A. & Strandberg, P. O. B. ( 1971; ). Carbonic anhydrase. In The Enzymes, vol. 5, pp. 587-665. Edited by P. D. Boyer. New York: Academic Press.
  33. McKay, R. M. L., Gibbs, S. P. & Espie, G. S. ( 1993; ). Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of Rubisco and the mode of inorganic carbon transport in cells of the cyanobacterium Synechococcus UTEX 625. Arch Microbiol 159, 21-29.[CrossRef]
    [Google Scholar]
  34. Malamy, M. H. & Horecker, B. L. ( 1964; ). Release of alkaline phosphatase from cells of Escherichia coli upon lysozyme sphaeroplast formation. Biochemistry 3, 172-175.
    [Google Scholar]
  35. Maren, T. H. & Sanyal, G. ( 1983; ). The activity of sulfonamides and anions against the carbonic anhydrase of animals, plants and bacteria. Annu Rev Pharmacol Toxicol 23, 439-459.[CrossRef]
    [Google Scholar]
  36. Monson, E. K., Ditta, G. S. & Helinski, D. R. ( 1995; ). The oxygen sensor protein, FixL, of Rhizobium meliloti. J Biol Chem 270, 5243-5250.[CrossRef]
    [Google Scholar]
  37. van Niel, C. B. ( 1944; ). The culture, general physiology, and classification of the non-sulfur purple and brown bacteria. Bacteriol Rev 8, 1-118.
    [Google Scholar]
  38. Perlman, D. & Halvorson, H. O. ( 1983; ). A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol 167, 391-409.[CrossRef]
    [Google Scholar]
  39. Price, G. D., Coleman, J. R. & Badger, M. R. ( 1992; ). Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100, 784-793.[CrossRef]
    [Google Scholar]
  40. Qian, Y. & Tabita, F. R. ( 1996; ). A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter sphaeroides. J Bacteriol 178, 12-18.
    [Google Scholar]
  41. Rawat, M. & Moroney, J. V. ( 1995; ). The regulation of carbonic anhydrase and ribulose 1,5-biphosphate carboxylase/oxygenase activase by light and CO2 in Chlamydomonas reinhardtii. Plant Physiol 109, 937-944.
    [Google Scholar]
  42. Smith, K. S., Jakubzick, C., Whittman, T. S. & Ferry, J. G. ( 1999; ). Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci USA 96, 15184-15189.[CrossRef]
    [Google Scholar]
  43. Soltes-Rak, E., Mulligan, M. E. & Coleman, J. R. ( 1997; ). Identification and characterization of a gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria. J Bacteriol 179, 769-774.
    [Google Scholar]
  44. Sugrue, M. F. ( 1996; ). The preclinical pharmacology of dorzolamide hydrochloride, a topical carbonic anhydrase inhibitor. J Ocul Pharmacol 12, 363-376.[CrossRef]
    [Google Scholar]
  45. Tabita, F. R. ( 1995; ). The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. In Anoxygenic Photosynthetic Bacteria: Advances in Photosynthesis, pp. 885-914. Edited by R. E. Blankenship, M. T. Madigan & C. E. Bauer. Dordrecht: Kluwer.
  46. Tai, S.-P. & Kaplan, S. ( 1985; ). Intracellular localization of phospholipid transfer activity in Rhodopseudomonas sphaeroides and a possible role in membrane biogenesis. J Bacteriol 164, 181-186.
    [Google Scholar]
  47. Tashian, R. E. ( 1989; ). The carbonic anhydrases: widening perspectives on their evolution, expression and function. BioEssays 10, 186-192.[CrossRef]
    [Google Scholar]
  48. Unden, G. & Schirawski, J. ( 1997; ). The oxygen-responsive transcriptional regulator FNR of Escherichia coli: the search for signals and reactions. Mol Microbiol 25, 205-210.[CrossRef]
    [Google Scholar]
  49. Vandenberg, J. I., Carter, N. D., Bethell, H. W. L., Nogradi, A., Ridderstrale, Y., Metcalfe, J. C. & Grace, A. A. ( 1996; ). Carbonic anhydrase and cardiac pH regulation. Am J Physiol 40, 1838-1846.
    [Google Scholar]
  50. Wilbur, K. M. & Anderson, N. G. ( 1948; ). Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 176, 147-154.
    [Google Scholar]
  51. Yu, J.-W., Price, G. D., Song, L. & Badger, M. R. ( 1992; ). Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synecochoccus PCC7942. Plant Physiol 100, 794-800.[CrossRef]
    [Google Scholar]
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