Copper starvation-inducible protein for cytochrome oxidase biogenesis in Bradyrhizobium japonicum

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38812-38823

  Serventi, Fabio ^a   Youard, Zeb Andrew ^a   Murset, Valérie ^a   Huwiler, Simona ^a   Bühler, Doris ^a   Richter, Miriam ^a   Luchsinger, Ronny ^a   Fischer, Hans Martin ^a   Brogioli, Robert ^a   Niederer, Martina ^a   Hennecke, Hauke ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYRHIZOBIUM JAPONICUM; COMPLEMENTATION; COPPER BINDING; COPPER TRANSPORT; CYTOCHROME OXIDASE; ENDOSYMBIOTIC; GENE PRODUCTS; HIGH AFFINITY; MICROARRAY ANALYSIS; NITRATE RESPIRATION; OUTER MEMBRANE; PERIPLASMIC PROTEINS; SOYBEAN ROOTS; SYMBIOTIC NITROGEN FIXATION;

AMINO ACIDS; BIOSYNTHESIS; CELL MEMBRANES; ESCHERICHIA COLI; GENES; NITROGEN FIXATION; PROTEINS; STOICHIOMETRY;

COPPER;

ALANINE; COPPER; CYTOCHROME C OXIDASE; HISTIDINE; METHIONINE; PCUA PROTEIN; PCUAC PROTEIN; PCUB PROTEIN; PCUC PROTEIN; PCUD PROTEIN; PCUE PROTEIN; PERIPLASMIC PROTEIN; SCOI PROTEIN; UNCLASSIFIED DRUG; YCNJ PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BINDING AFFINITY; BIOGENESIS; BRADYRHIZOBIUM JAPONICUM; CONTROLLED STUDY; DENITRIFICATION; ESCHERICHIA COLI; GENE DELETION; GENETIC REGULATION; GENETIC TRANSCRIPTION; MICROARRAY ANALYSIS; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PCUA GENE; PCUB GENE; PCUC GENE; PCUD GENE; PCUE GENE; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; STOICHIOMETRY; SYMBIOSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BRADYRHIZOBIUM; CARRIER PROTEINS; COPPER; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; MITOCHONDRIAL PROTEINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTATION; NITROGEN; NITROGEN FIXATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PERIPLASM; PHENOTYPE; SEQUENCE HOMOLOGY, AMINO ACID;

BRADYRHIZOBIUM JAPONICUM; ESCHERICHIA COLI; GLYCINE MAX;

EID: 84869070822     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.406173     Document Type: Article

References (63)

1. García-Horsman, J. A., Barquera, B., Rumbley, J., Ma, J., and Gennis, R. B. (1994) The superfamily of heme-copper respiratory oxidases. J. Bacteriol. 176, 5587-5600 (Pubitemid 24280490)
2. Sousa, F. L., Alves, R. J., Ribeiro, M. A., Pereira-Leal, J. B., Teixeira, M., and Pereira, M. M. (2012) The superfamily of heme-copper oxygen reductases. Types and evolutionary considerations. Biochim. Biophys. Acta 1817, 629-637
3. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., Puustinen, A., Iwata, S., and Wikström, M. (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat. Struct. Biol. 7, 910-917
4. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660-669
5. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272, 1136-1144
6. 3 oxidases are an ancient innovation of the domain bacteria. Mol. Biol. Evol. 25, 1158-1166
7. 3 cytochrome oxidase provides insights into proton pumping. Science 329, 327-330
8. Poole, R. K., and Cook, G. M. (2000) Redundancy of aerobic respiratory chains in bacteria? Routes, reasons, and regulation. Adv. Microb. Physiol. 43, 165-224 (Pubitemid 30481125)
9. 2 environments. Proc. Natl. Acad. Sci. U.S.A. 108, 14109-14114
10. Bühler, D., Rossmann, R., Landolt, S., Balsiger, S., Fischer, H. M., and Hennecke, H. (2010) Disparate pathways for the biogenesis of cytochrome oxidases in Bradyrhizobium japonicum. J. Biol. Chem. 285, 15704-15713
11. van der Oost, J., Haltia, T., Raitio, M., and Saraste, M. (1991) Genes coding for cytochrome c oxidase in Paracoccus denitrificans. J. Bioenerg. Biomembr. 23, 257-267
12. B and magnesium centers of cytochrome c oxidase. J. Biol. Chem. 275, 619-623
13. Cobine, P. A., Pierrel, F., and Winge, D. R. (2006) Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim. Biophys. Acta 1763, 759-772 (Pubitemid 44189537)
14. B of cytochrome c oxidase. Biochemistry 49, 5651-5661
15. 3-type cytochrome c oxidase in Rhodobacter capsulatus. Biochim. Biophys. Acta 1817, 898-910
16. Hassani, B. K., Astier, C., Nitschke, W., and Ouchane, S. (2010) CtpA, a copper-translocating P-type ATPase involved in the biogenesis of multiple copper-requiring enzymes. J. Biol. Chem. 285, 19330-19337
17. Preisig, O., Zufferey, R., and Hennecke, H. (1996) The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high affinity cbb3-type cytochrome oxidase. Arch. Microbiol. 165, 297-305 (Pubitemid 26175058)
18. 3-type cytochrome c oxidase. J. Mol. Biol. 297, 49-65
19. Robinson, N. J., and Winge, D. R. (2010) Copper metallochaperones. Annu. Rev. Biochem. 79, 537-562
20. A center of cytochrome c oxidase. Biochemistry 48, 4448-4454
21. Arunothayanan, H., Nomura, M., Hamaguchi, R., Itakura, M., Minamisawa, K., and Tajima, S. (2010) Copper metallochaperones are required for the assembly of bacteroid cytochrome c oxidase which is functioning for nitrogen fixation in soybean nodules. Plant Cell Physiol. 51, 1242-1246
22. Frangipani, E., and Haas, D. (2009) Copper acquisition by the SenC protein regulates aerobic respiration in Pseudomonas aeruginosa PAO1. FEMS Microbiol. Lett. 298, 234-240
23. 3-type cytochrome oxidase in Rhodobacter capsulatus. Biochim. Biophys. Acta 1817, 2005-2015
24. 3-type cytochrome c oxidases. Biochim. Biophys. Acta 1817, 955-964
25. A assembly. Nat. Chem. Biol. 4, 599-601
26. Miller, J. H. (1972) Experiments in Molecular Genetics, p. 433, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
27. Regensburger, B., and Hennecke, H. (1983) RNA polymerase from Rhizobium japonicum. Arch. Microbiol. 135, 103-109
28. 1 cascade in Bradyrhizobium japonicum. J. Bacteriol. 190, 6568-6579
29. Vincent, J. M. (1970) A Manual for the Practical Study of Root Nodule Bacteria, Blackwell Scientific, Oxford, UK
30. Becker, A., Bergès, H., Krol, E., Bruand, C., Rüberg, S., Capela, D., Lauber, E., Meilhoc, E., Ampe, F., de Bruijn, F. J., Fourment, J., Francez-Charlot, A., Kahn, D., Küster, H., Liebe, C., Pühler, A., Weidner, S., and Batut, J. (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol. Plant Microbe Interact. 17, 292-303 (Pubitemid 38403228)
31. Bishop, P. E., Guevara, J. G., Engelke, J. A., and Evans, H. J. (1976) Relation between glutamine synthetase and nitrogenase activities in the symbiotic association between Rhizobium japonicum and Glycine max. Plant Physiol. 57, 542-546
32. Daniel, R. M., and Appleby, C. A. (1972) Anaerobic-nitrate, symbiotic and aerobic growth of Rhizobium japonicum. Effects on cytochrome P450, other hemoproteins, nitrate, and nitrite reductases. Biochim. Biophys. Acta 275, 347-354
33. 3 branch of the Bradyrhizobium japonicum respiratory chain. Mol. Microbiol. 4, 2147-2157
34. Preisig, O., Anthamatten, D., and Hennecke, H. (1993) Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. U.S.A. 90, 3309-3313 (Pubitemid 23111355)
35. Fischer, H. M., Babst, M., Kaspar, T., Acuña, G., Arigoni, F., and Hennecke, H. (1993) One member of a groESL-like chaperonin multigene family in Bradyrhizobium japonicum is co-regulated with symbiotic nitrogen fixation genes. EMBO J. 12, 2901-2912 (Pubitemid 23218340)
36. Higuchi, R., Krummel, B., and Saiki, R. K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments. Study of protein and DNA interactions. Nucleic Acids Res. 16, 7351-7367
37. 54 regulon and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation. Mol. Genet. Genomics 278, 255-271
38. Lindemann, A., Moser, A., Pessi, G., Hauser, F., Friberg, M., Hennecke, H., and Fischer, H. M. (2007) New target genes controlled by the Bradyrhizobium japonicum two-component regulatory system RegSR. J. Bacteriol. 189, 8928-8943
39. Beck, C., Marty, R., Kläusli, S., Hennecke, H., and Göttfert, M. (1997) Dissection of the transcription machinery for housekeeping genes of Bradyrhizobium japonicum. J. Bacteriol. 179, 364-369 (Pubitemid 27030388)
40. 2, a key regulator for the Bradyrhizobium japonicum-soybean symbiosis. Proc. Natl. Acad. Sci. U.S.A. 106, 21860-21865
41. Hahn, M., and Hennecke, H. (1984) Localized mutagenesis in Rhizobium japonicum. Mol. Gen. Genet. 193, 46-52 (Pubitemid 14176169)
42. Göttfert, M., Grob, P., and Hennecke, H. (1990) Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U.S.A. 87, 2680-2684 (Pubitemid 20141803)
43. Göttfert, M., Hitz, S., and Hennecke, H. (1990) Identification of nodS and nodU, two inducible genes inserted between the Bradyrhizobium japonicum nodYABC and nodIJ genes. Mol. Plant Microbe Interact. 3, 308-316
44. Sarma, A. D., and Emerich, D. W. (2005) Global protein expression pattern of Bradyrhizobium japonicum bacteroids. A prelude to functional proteomics. Proteomics 5, 4170-4184 (Pubitemid 41626085)
45. Delmotte, N., Ahrens, C. H., Knief, C., Qeli, E., Koch, M., Fischer, H. M., Vorholt, J. A., Hennecke, H., and Pessi, G. (2010) An integrated proteomics and transcriptomics reference data set provides new insights into the Bradyrhizobium japonicum bacteroid metabolism in soybean root nodules. Proteomics 10, 1391-1400
46. Nicholas, D. J. D., and Nason, A. (1957) Determination of nitrate and nitrite. Methods Enzymol. 3, 981-984
47. 1 gene replacement mutants. J. Bacteriol. 172, 2392-2400
48. Bradford, M. M. (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
49. Loferer, H., Bott, M., and Hennecke, H. (1993) Bradyrhizobium japonicum TlpA, a novel membrane-anchored thioredoxin-like protein involved in the biogenesis of cytochrome aa3 and development of symbiosis. EMBO J. 12, 3373-3383 (Pubitemid 23256424)
50. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
51. Parks, T. D., Leuther, K. K., Howard, E. D., Johnston, S. A., and Dougherty, W. G. (1994) Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase. Anal. Biochem. 216, 413-417 (Pubitemid 24076026)
52. Schulz, H., Hennecke, H., and Thöny-Meyer, L. (1998) Prototype of a heme chaperone essential for cytochrome c maturation. Science 281, 1197-1200 (Pubitemid 28406296)
53. Kapust, R. B., Tözsér, J., Fox, J. D., Anderson, D. E., Cherry, S., Copeland, T. D., and Waugh, D. S. (2001) Tobacco etch virus protease. Mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng. 14, 993-1000 (Pubitemid 34137240)
54. Zhou, L., Singleton, C., and Le Brun, N. E. (2008) High Cu(I) and low proton affinities of the CXXC motif of Bacillus subtilis CopZ. Biochem. J. 413, 459-465
55. Krewulak, K. D., and Vogel, H. J. (2011) TonB or not TonB. Is that the question? Biochem. Cell Biol. 89, 87-97
56. Bender, C. L., and Cooksey, D. A. (1986) Indigenous plasmids in Pseudomonas syringae pv. tomato. Conjugative transfer and role in copper resistance. J. Bacteriol. 165, 534-541 (Pubitemid 16060526)
57. Chillappagari, S., Miethke, M., Trip, H., Kuipers, O. P., and Marahiel, M. A. (2009) Copper acquisition is mediated by YcnJ and regulated by YcnK and CsoR in Bacillus subtilis. J. Bacteriol. 191, 2362-2370
58. Velasco, L., Mesa, S., Delgado, M. J., and Bedmar, E. J. (2001) Characterization of the nirK gene encoding the respiratory, copper-containing nitrite reductase of Bradyrhizobium japonicum. Biochim. Biophys. Acta 1521, 130-134 (Pubitemid 33020775)
59. Smith, G. F., and Wilkins, D. H. (1953) New colorimetric reagent specific for copper. Anal. Chem. 25, 510-511
60. Zak, B. (1958) Simple procedure for the single sample determination of serum copper and iron. Clin. Chim. Acta 3, 328-334
61. 3-type cytochrome c oxidase in Rhodobacter capsulatus. MBio 10.1128/mBio.00293-11
62. Banci, L., Bertini, I., Ciofi-Baffoni, S., Kozyreva, T., Zovo, K., and Palumaa, P. (2010) Affinity gradients drive copper to cellular destinations. Nature 465, 645-648
63. 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J. Bacteriol. 178, 1532-1538