Comparative biochemical and functional studies of family I soluble inorganic pyrophosphatases from photosynthetic bacteria

FEBS Journal

Volumn 274, Issue 15, 2007, Pages 3948-3959

  Gómez García, María R ^a,b   Losada, Manuel ^a   Serrano, Aurelio ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Anoxygenic photosynthetic bacteria; Cyanobacteria; Functional complementation; ppa; Soluble pyrophosphatases

Indexed keywords

BACTERIAL ENZYME; ENZYME ANTIBODY; INORGANIC PYROPHOSPHATASE; MAGNESIUM ION; OLIGOMER;

AMINO ACID SEQUENCE; ANABAENA; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM; BACTERIUM MUTANT; BLASTOCHLORIS VIRIDIS; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS REACTION; CYANOBACTERIUM; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; GENE FUNCTION; HELIOBACTERIUM; HETEROLOGOUS EXPRESSION; IMMUNOHISTOCHEMISTRY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PSEUDANABAENA; SYNECHOCYSTIS; WILD TYPE;

CHLOROBI; CHROMATIACEAE; CHROMATOGRAPHY, GEL; CYANOBACTERIA; GRAM-NEGATIVE BACTERIA; INORGANIC PYROPHOSPHATASE; KINETICS; OXYGEN; PHOTOSYNTHESIS; PHYLOGENY; SOLUBILITY;

BACTERIA (MICROORGANISMS); BLASTOCHLORIS VIRIDIS; CYANOBACTERIA; ESCHERICHIA COLI; NOSTOC SP. PCC 7120; PHOTOBACTERIA; PROKARYOTA; PSEUDANABAENA SP. PCC 6903; SYNECHOCYSTIS SP. PCC 6803;

EID: 34447644066     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05927.x     Document Type: Article

References (47)

1. Kornberg A (1962) On the metabolic significance of phosphorolytic and pyrophosphorolytic reactions. In Horizons in Biochemistry (Kasha M Pullman D, eds), pp. 251 254. Academic Press, New York, NY.
2. Cooperman BS, Baykov AA Lahti R (1992) Evolutionary conservation of the active site of soluble inorganic pyrophosphatase. Trends Biochem Sci 17, 262 266.
3. Young TW, Kuhn NJ, Wadeson A, Ward S, Burges D Cooke GD (1998) Bacillus subtilis ORF yybQ encodes a manganese-dependent inorganic pyrophosphatase with distinctive properties: the first of a new class of soluble pyrophosphatase? Microbiology 144, 2563 2571.
4. Shintani T, Uchiumi T, Yonezawa T, Salminen A, Baykov AA, Lahti R Hachimori A (1998) Cloning and expression of a unique inorganic pyrophosphatase from Bacillus subtilis: evidence for a new family of enzymes. FEBS Lett 439, 263 266.
5. Parfenyev AN, Salminen A, Halonen P, Hachimori A, Baykov AA Lahti R (2001) Quaternary structure and metal ion requirement of family II pyrophosphatases from Bacillus subtilis, Streptococcus gordonii, and Streptococcus mutans. J Biol Chem 276, 24511 24518.
6. Zyryanov AB, Vener AV, Salminen A, Goldman A, Lahti R Baykov AA (2004) Rates of elementary catalytic steps for different metal forms of the family II pyrophosphatase from Streptococcus gordonii. Biochemistry 43, 1065 1074.
7. Heikinheimo P, Lehtonen J, Baykov A, Lahti R, Cooperman BS Goldman A (1996) The structural basis for pyrophosphatase catalysis. Structure 4, 1491 1508.
8. Harutyunyan EH, Kuranova IP, Vainshtein BK, Höhne WE, Lamzin VS, Dauter Z, Teplyakov AV Wilson KS (1996) X-ray structure of yeast inorganic pyrophosphatase complexed with manganese and phosphate. Eur J Biochem 239, 220 228.
9. Merckel MC, Fabrichniy IP, Salminen A, Kalkkinen N, Baykov AA, Lahti R Goldman A (2001) Crystal structure of Streptococcus mutants pyrophosphatase: a new fold for an old mechanism. Structure 9, 289 297.
10. Ahn S, Milner AJ, Fütterer K, Konopka M, Ilias M, Young TW White SA (2001) The open and closed structures of the type-C inorganic pyrophosphatases from Bacillus subtilis and Streptococcus gordonii. J Mol Biol 313, 797 811.
11. Baykov AA, Cooperman B, Goldman A Lahti R (1999) Cytoplasmic inorganic pyrophosphatase. Prog Mol Subcell Biol 23, 127 150.
12. Gómez-García MR, Losada M Serrano A (2006) A novel subfamily of monomeric inorganic pyrophosphatases in photosynthetic eukaryotes. Biochem J 395, 211 221.
13. Perez-Castineira JR, Gomez-Garcia R, Lopez-Marques RL, Losada M Serrano A (2001) Enzymatic systems of inorganic pyrophosphate bioenergetics in photosynthetic and heterotrophic protists: remnants or metabolic cornerstones? Int Microbiol 4, 135 142.
14. Serrano A, Perez-Castineira JR, Baltscheffsky H Baltscheffsky M (2004) Proton-pumping inorganic pyrophosphatases in some archaea and other extremophilic prokaryotes. J Bioenerg Biomembr 36, 127 133.
15. Serrano A, Perez-Castineira JR, Baltscheffsky M Baltscheffsky H (2007) H+-PPases: yesterday, today and tomorrow. IUBMB Life 59, 76 83.
16. Kang CB Ho KK (1991) Characterization of a soluble inorganic pyrophosphatase from Microcystis aeruginosa and preparation of its antibody. Arch Biochem Biophys 289, 281 288.
17. Rippka R, Deruelles J, Waterbury JB, Herdman M Stanier RY (1979) Generic assignment, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111, 1 61.
18. Kankare J, Neal GS, Salminen T, Glumoff T, Glumhoff T, Cooperman BS, Lahti R Goldman A (1994) The structure of E. coli soluble inorganic pyrophosphatase at 2.7Å resolution. Protein Eng 7, 823 830.
19. Efimova IS, Salminen A, Pohjanjoki P, Lapinniemi J, Magretova NN, Cooperman BS, Goldman A, Lahti R Baykov AA (1999) Directed mutagenesis studies of the metal binding site at the subunit interface of Escherichia coli inorganic pyrophosphatase. J Biol Chem 274, 3294 3299.
20. Salminen A, Kapyla TJ, Heikinheimo P, Kankare J, Goldman A, Heinonen J, Baykov AA, Cooperman BS Lahti R (1995) Structure and function analysis of Escherichia coli inorganic pyrophosphatase: is a hydroxide ion the key to catalysis? Biochemistry 34, 782 791.
21. Celis H, Franco B, Escobedo S Romero I (2003) Rhodobacter sphaeroides has a family II pyrophosphatase: comparison with other species of photosynthetic bacteria. Arch Microbiol 179, 368 376.
22. Gómez-García MR, Losada M Serrano A (2002) Expression studies of two paralogous ppa genes encoding distinct family I pyrophosphatases in marine unicellular cyanobacteria reveal inactivation of the typical cyanobacterial gene. Biochem Biophys Res Commun 295, 890 897.
23. Lawrence JG, Hendris RW Casjens S (2001) Where are the pseudogenes in bacterial genomes? Trends Microbiol 9, 535 540.
24. Klemme JH, Klemme B Gest H (1971) Catalytic properties and regulatory diversity of inorganic pyrophosphatases from photosynthetic bacteria. J Bacteriol 108, 1122 1128.
25. Olson JM (1970) Evolution of photosynthesis re-examined thirty years later. Photosynth Res 68, 95 112.
26. Chen J, Brevet A, Fromant M, Lévêque F, Schmitter JM, Blanquet S Plateau P (1990) Pyrophosphatase is essential for growth of Escherichia coli. J Bacteriol 172, 5686 5689.
27. Gómez-García MR, Losada M Serrano A (2003) Concurrent transcriptional activation of ppa and ppx genes by phosphate deprivation in the cyanobacterium Synechocystis sp. strain PCC 6803. Biochem Biophys Res Commun 302, 601 609.
28. Mitchell SJ Minnick MF (1997) Cloning, functional expression, and complementation analysis of an inorganic pyrophosphatase from Bartonella bacilliformis. Can J Microbiol 43, 734 743.
29. Lahti R, Perala M, Heikinheimo P, Pitkaranta T, Kukko-Kalske E Heinonen J (1991a) Characterization of the 5′ flanking region of the Escherichia coli ppa gene encoding inorganic pyrophosphatase: mutations in the ribosome-binding site decrease the level of ppa mRNA. J Gen Microbiol 137, 2517 2523.
30. Kukko-Kalske E Heinonen J (1985) Inorganic pyrophosphate and inorganic pyrophosphatase in Escherichia coli. Int J Biochem 17, 575 580.
31. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S et al. (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803 PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3, 109 136.
32. Gingrich JC, Gasparich GE, Sauer K Bryant DA (1989) Nucleotide sequence and expression of the two genes encoding D2 protein and the single gene encoding the CP43 protein of photosystem II in the cyanobacterium Synechococcus sp. PCC 7002. Photosynthesis Res 24, 137 150.
33. Cohen-Bazire G, Sistrom WR Stanier RY (1957) Kinetic studies of pigment synthesis by non-sulphur purple bacteria. J Cell Comp Physiol 49, 25 68.
34. Pfenning N Trüper HG (1991) The family Chromatiaceae. In The Prokaryotes (Balows A, Trüper HG, Dworkin M, Harder W Schleifer KH, eds), pp. 3200 3221. Springer, Berlin.
35. Gest H Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a 'new' form of bacterio chlorophyll. Arch Microbiol 136, 11 16.
36. Lahti R, Pikaranta T, Valve E, Ilta I, Kukko-Kalse E Heinonen J (1988) Cloning and characterization of the gene encoding inorganic pyrophosphatase of Escherichia coli K-12. J Bacteriol 170, 5901 5907.
37. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557 580.
38. Fiske CH Subarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66, 375 400.
39. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248 254.
40. Harlow E Lane D (1988) Antibodies: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, NY.
41. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA Struhl K (1985) Current Protocols in Molecular Biology. John Wiley & Sons, New York, NY.
42. Linden H, Vioque A Sandman G (1987) Isolation of a carotenoid biosynthesis gene coding for ζ-carotene desaturase from Anabaena PCC 7120 by heterologous complementation. FEMS Microbiol Lett 106, 99 104.
43. Crespo JL, García-Domínguez M Florencio FJ (1998) Nitrogen control of the glnN gene that codes for GS type III, the only glutamine synthetase in the cyanobacterium Pseudanabaena sp. PCC 6903. Mol Microbiol 30, 1101 1112.
44. Cai YP Wolk CP (1990) Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172, 3138 3145.
45. Church GM Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81, 1991 1995.
46. Thompson JD, Gibson TJ, Plewnisk F, Jeanmougin F Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876 4882.
47. Altschul SF, Madden MT, Schaffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res Rev 25, 3389 33402.