The extracellular heme-binding protein hbps from the soil bacterium Streptomyces reticuli is an aquo-cobalamin binder

Journal of Biological Chemistry

Volumn 289, Issue 49, 2014, Pages 34214-34228

  De Orué Lucana, Darío Ortiz ^a   Fedosov, Sergey N ^b   Wedderhoff, Ina ^a   Che, Edith N ^a   Torda, Andrew E ^c  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; METAL IONS; PORPHYRINS; PROTEINS; SOIL TESTING; ULTRAVIOLET VISIBLE SPECTROSCOPY;

COORDINATING LIGANDS; EXTRACELLULAR PROTEINS; GRAM-NEGATIVE BACTERIA; HISTIDINE RESIDUES; SENSING SYSTEMS; SEQUENCE COMPARISONS; SOIL BACTERIUM; UV VISIBLE SPECTROSCOPY;

BACTERIA;

BACTERIAL PROTEIN; COBALT; HEMOPROTEIN; HISTIDINE; HYDROXOCOBALAMIN; PROTEIN HBPS; UNCLASSIFIED DRUG; CARRIER PROTEIN; CYANOCOBALAMIN; HEME; HEME-BINDING PROTEIN; IRON; PROTEIN BINDING; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIUM CULTURE; BINDING AFFINITY; BINDING COMPETITION; CONTROLLED STUDY; MOLECULAR CLONING; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SOIL MICROFLORA; STREPTOMYCES RETICULI; ULTRAVIOLET SPECTROSCOPY; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; SEQUENCE ALIGNMENT; STREPTOMYCES; STRUCTURAL HOMOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA; STREPTOMYCES RETICULI;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BINDING, COMPETITIVE; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE EXPRESSION; HEME; HEMEPROTEINS; HISTIDINE; IRON; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SOIL MICROBIOLOGY; STREPTOMYCES; STRUCTURAL HOMOLOGY, PROTEIN; VITAMIN B 12;

EID: 84917710534     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.585489     Document Type: Article

References (69)

1. Pratt, J. M. (1972) Inorganic Chemistry of Vitamin B12. Academic Press, Inc. London
2. Kräutler, B. (2005) Vitamin B12: chemistry and biochemistry. Biochem. Soc. Trans. 33, 806-810
3. Lochhead, A. G., and Thexton, R. H. (1951) Vitamin B12 as a growth factor for soil bacteria. Nature 167, 1034
4. Lochhead, A. G., and Burton, M. O. (1956) Soil as a habitat of vitaminrequiring bacteria. Nature 178, 144-145
5. Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J., and Smith, A. G. (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90-93
6. Mozafar, A., and Oertli, J. J. (1992) Uptake of a microbially-produced vitamin (B12) by soybean roots. Plant Soil 139, 23-30
7. Friedmann, H. C., and Cagen, L. M. (1970) Microbial biosynthesis of B12-like compounds. Annu. Rev. Microbiol. 24, 159-208
8. Roth, J. R., Lawrence, J. G., Rubenfield, M., Kieffer-Higgins, S., and Church, G. M. (1993) Characterization of the cobalamin (vitamin B12) biosynthetic genes of Salmonella typhimurium. J. Bacteriol. 175, 3303-3316
9. Roth, J. R., Lawrence, J. G., and Bobik, T. A. (1996) Cobalamin (coenzyme B12): synthesis and biological significance. Annu. Rev. Microbiol. 50, 137-181
10. Warren, M. J., Raux, E., Schubert, H. L., and Escalante-Semerena, J. C. (2002) The biosynthesis of adenosylcobalamin (vitamin B12). Nat. Prod. Rep. 19, 390-412
11. Meschke, H., and Schrempf, H. (2010) Streptomyces lividans inhibits the proliferation of the fungus Verticillium dahliae on seeds and roots of Arabidopsis thaliana. Microb. Biotechnol. 3, 428-443
12. Book, A. J., Lewin, G. R., McDonald, B. R., Takasuka, T. E., Doering, D. T., Adams, A. S., Blodgett, J. A., Clardy, J., Raffa, K. F., Fox, B. G., and Currie, C. R. (2014) Cellulolytic Streptomyces strains associated with herbivorous insects share a phylogenetically-linked capacity for the degradation of lignocellulose. Appl. Environ. Microbiol. 80, 4692-4701
13. Chater, K. F., Biró, S., Lee, K. J., Palmer, T., and Schrempf, H. (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol. Rev. 34, 171-198
14. Gruber, K., Puffer, B., and Kräutler, B. (2011) Vitamin B12-derivativesenzyme cofactors and ligands of proteins and nucleic acids. Chem. Soc. Rev. 40, 4346-4363
15. Fedosov, S. N., Fedosova, N. U., Kräutler, B., Nexø, E., and Petersen, T. E. (2007) Mechanisms of discrimination between cobalamins and their natural analogues during their binding to the specific B12-transporting proteins. Biochemistry 46, 6446-6458
16. Kräutler, B. (2006) Cobalt: B12 enzymes and coenzymes. Encyclopedia of Inorganic Chemistry
17. Flinspach, K., Westrich, L., Kaysser, L., Siebenberg, S., Gomez-Escribano, J. P., Bibb, M., Gust, B., and Heide, L. (2010) Heterologous expression of the biosynthetic gene clusters of coumermycin A(1), clorobiocin, and caprazamycins in genetically modified Streptomyces coelicolor strains. Biopolymers 93, 823-832
18. Allen, K. D., and Wang, S. C. (2014) Initial characterization of Fom3 from Streptomyces wedmorensis: the methyltransferase in fosfomycin biosynthesis. Arch. Biochem. Biophys. 543, 67-73
19. Borovok, I., Gorovitz, B., Schreiber, R., Aharonowitz, Y., and Cohen, G. (2006) Coenzyme B12 controls transcription of the Streptomyces class Ia ribonucleotide reductase nrdABS operon via a riboswitch mechanism. J. Bacteriol. 188, 2512-2520
20. Hoffmann, B., Konrat, R., Bothe, H., Buckel, W., and Kräutler, B. (1999) Structure and dynamics of the B12-binding subunit of glutamate mutase from Clostridium cochlearium. Eur. J. Biochem. 263, 178-188
21. Sjuts, H., Dunstan, M. S., Fisher, K., and Leys, D. (2013) Structure of the cobalamin-binding protein of a putative O-demethylase from Desulfitobacterium hafniense DCB-2. Acta Crystallogr. D Biol. Crystallogr. 69, 1609-1616
22. Shibata, N., Masuda, J., Tobimatsu, T., Toraya, T., Suto, K., Morimoto, Y., and Yasuoka, N. (1999) A new mode of B12 binding and the direct participation of a potassium ion in enzyme catalysis: x-ray structure of diol dehydratase. Structure 7, 997-1008
23. Wuerges, J., Garau, G., Geremia, S., Fedosov, S. N., Petersen, T. E., and Randaccio, L. (2006) Structural basis for mammalian vitamin B12 transport by transcobalamin. Proc. Natl. Acad. Sci. U.S.A. 103, 4386-4391
24. Wuerges, J., Geremia, S., Fedosov, S. N., and Randaccio, L. (2007) Vitamin B12 transport proteins: crystallographic analysis of beta-axial ligand substitutions in cobalamin bound to transcobalamin. IUBMB Life 59, 722-729
25. Wedderhoff, I., Kursula, I., Groves, M. R., and Ortiz de Orué Lucana, D. (2013) Iron binding at specific sites within the octameric HbpS protects streptomycetes from iron-mediated oxidative stress. PLoS One 8, e71579
26. Ortiz de Orué Lucana, D., Schaa, T., and Schrempf, H. (2004) The novel extracellular Streptomyces reticuli heme-binding protein HbpS influences the production of the catalase-peroxidase CpeB. Microbiology 150, 2575-2585
27. Torda, A. E., Groves, M. R., Wedderhoff, I., and Ortiz de Orué Lucana, D. (2013) Elucidation of heme-binding sites in the actinobacterial protein HbpS. FEMS Microbiol. Lett. 342, 106-112
28. Ortiz de Orué Lucana, D., Bogel, G., Zou, P., and Groves, M. R. (2009) The oligomeric assembly of the novel heme-degrading protein HbpS is essential for interaction with its cognate two-component sensor kinase. J. Mol. Biol. 386, 1108-1122
29. Ortiz de Orué Lucana, D., Roscher, M., Honigmann, A., and Schwarz, J. (2010) Iron-mediated oxidation induces conformational changes within the redox-sensing protein HbpS. J. Biol. Chem. 285, 28086-28096
30. Ortiz de Orué Lucana, D., and Groves, M. R. (2009) The three-component signalling system HbpS-SenS-SenR as an example of a redox sensing pathway in bacteria. Amino Acids 37, 479-486
31. Siedenburg, G., Groves, M. R., and Ortiz de Orué Lucana, D. (2012) Novel redox-sensing modules: accessory proteins- and nucleic acids-mediated signaling. Antioxid. Redox. Signal. 16, 668-677
32. Zou, P., Groves, M. R., Viale-Bouroncle, S. D., and Ortiz de Orué Lucana, D. (2008) Cristallization and preliminary characterization of a novel heme-binding protein of Streptomyces reticuli. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64, 386-390
33. Hopwood, D. A., Bibb, M. J., Chater, K. F., Kieser, T., Bruton, C. J., Kieser, H. M., Lydiate, D. J., Smith, C. P., Ward, J. M., and Schrempf, H. (1985) Genetic Manipulation of Streptomyces: A Laboratory Manual, John Innes Foundation, Norwich, UK
34. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2 Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
35. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 72, 248-254
36. Dawson, J. H., Andersson, L. A., and Sono, M. (1983) The diverse spectroscopic properties of ferrous cytochrome P-450-CAM ligand complexes. J. Biol. Chem. 258, 13637-13645
37. Hargrove, M. S., Singleton, E. W., Quillin, M. L., Ortiz, L. A., Phillips, G. N. Jr., Olson, J. S., Mathews, A. J. (1994) His64(E7)→Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation. J. Biol. Chem. 269, 4207-4214
38. Bhakta, M. N., and Wilks, A. (2006) The mechanism of heme transfer from the cytoplasmic heme binding protein PhuS to the delta-regioselective heme oxygenase of Pseudomonas aeruginosa. Biochemistry 45, 11642-11649
39. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
40. Katoh, K., and Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780
41. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313
42. Huson, D. H., and Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254-267
43. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539
44. Fedosov, S. N., Fedosova, N. U., Nexø, E., and Petersen, T. E. (2000) Conformational changes of transcobalamin induced by aquocobalamin binding: mechanism of substitution of the cobalt-coordinated group in the bound ligand. J. Biol. Chem. 275, 11791-11798
45. Fedosov, S. N., Fedosova, N. U., Berglund, L., Moestrup, S. K., Nexø, E., and Petersen, T. E. (2005) Composite organization of the cobalamin binding and cubilin recognition sites of intrinsic factor. Biochemistry 44, 3604-3614
46. Nexo, E. (1975) A new principle in biospecific affinity chromatography used for purification of cobalamin-binding proteins. Biochim. Biophys. Acta 379, 189-192
47. Fedosov, S. N., Laursen, N. B., Nexø, E., Moestrup, S. K., Petersen, T. E., Jensen, E. Ø., and Berglund, L. (2003) Human intrinsic factor expressed in the plant Arabidopsis thaliana. Eur. J. Biochem. 270, 3362-3367
48. de Villiers, K. A., Kaschula, C. H., Egan, T. J., and Marques, H. M. (2007) Speciation and structure of ferriprotoporphyrin IX in aqueous solution: spectroscopic and diffusion measurements demonstrate dimerization, but not mu-oxo dimer formation. J. Biol. Inorg. Chem. 12, 101-117
49. Asher, C., de Villiers, K. A., and Egan, T. J. (2009) Speciation of ferriprotoporphyrin IX in aqueous and mixed aqueous solution is controlled by solvent identity, pH, and salt concentration. Inorg. Chem. 48, 7994-8003
50. Fedosov, S. N., Berglund, L., Nexo, E., and Petersen, T. E. (1999) Comparative analysis of cobalamin binding kinetics and ligand protection for intrinsic factor, transcobalamin and haptocorrin. J. Biol. Chem. 274, 26015-26020
51. Mozafar, A. (1994) Enrichment of some B-vitamins in plants with application of organic fertilizers. Plant Soil 167, 305-311
52. Martens, J. H., Barg, H., Warren, M. J., and Jahn, D. (2002) Microbial production of vitamin B12. Appl. Microbiol. Biotechnol. 58, 275-285
53. Hargrove, M. S., Barrick, D., Olson, J. S. (1996) The association rate constant for heme binding to globin is independent of protein structure. Biochemistry 35, 11293-11299
54. Yukl, E. T., Jepkorir, G., Alontaga, A. Y., Pautsch, L., Rodriguez, J. C., Rivera, M., and Moënne-Loccoz, P. (2010) Kinetic and spectroscopic studies of hemin acquisition in the hemophore HasAp from Pseudomonas aeruginosa. Biochemistry 49, 6646-6654
55. Deniau, C., Gilli, R., Izadi-Pruneyre, N., Létoffé, S., Delepierre, M., Wandersman, C., Briand, C., and Lecroisey, A. (2003) Thermodynamics of heme binding to the HasA(SM) hemophore: effect of mutations at three key residues for heme uptake. Biochemistry 42, 10627-10633
56. Nygaard, T. K., Blouin, G. C., Liu, M., Fukumura, M., Olson, J. S., Fabian, M., Dooley, D. M., and Lei, B. (2006) The mechanism of direct heme transfer from the streptococcal cell surface protein Shp to HtsA of the HtsABC transporter. J. Biol. Chem. 281, 20761-20771
57. Owens, C. P., Du, J., Dawson, J. H., and Goulding, C. W. (2012) Characterization of heme ligation properties of Rv0203, a secreted heme binding protein involved in Mycobacterium tuberculosis heme uptake. Biochemistry 51, 1518-1531
58. Kuznets, G., Vigonsky, E., Weissman, Z., Lalli, D., Gildor, T., Kauffman, S. J., Turano, P., Becker, J., Lewinson, O., and Kornitzer, D. (2014) A relay network of extracellular heme-binding proteins drives C. albicans iron acquisition from hemoglobin. PLoS Pathog. 10, e1004407
59. Yin, L., Dragnea, V., Feldman, G., Hammad, L. A., Karty, J. A., Dann, C. E., 3rd, and Bauer, C. E. (2013) Redox and light control the heme-sensing activity of AppA. MBio. 4, e00563-13
60. Yin, L., Dragnea, V., and Bauer, C. E. (2012) PpsR, a regulator of heme and bacteriochlorophyll biosynthesis, is a heme-sensing protein. J. Biol. Chem. 287, 13850-13858
61. Cho, H. Y., Cho, H. J., Kim, Y. M., Oh, J. I., and Kang, B. S. (2009) Structural insight into the heme-based redox sensing by DosS from Mycobacterium tuberculosis. J. Biol. Chem. 284, 13057-13067
62. Podust, L. M., Ioanoviciu, A., and Ortiz de Montellano, P. R. (2008) 2.3 Å x-ray structure of the heme-bound GAF domain of sensory histidine kinase DosT of Mycobacterium tuberculosis. Biochemistry 47, 12523-12531
63. Bogel, G., Schrempf, H., and Ortiz de Orué Lucana, D. (2009) The hemebinding protein HbpS regulates the activity of the Streptomyces reticuli iron-sensing histidine kinase SenS in a redox-dependent manner. Amino Acids 37, 681-691
64. Walsh, C. T., Garneau-Tsodikova, S., and Howard-Jones, A. R. (2006) Biological formation of pyrroles: nature's logic and enzymatic machinery. Nat. Prod. Rep. 23, 517-531
65. Romero, D., Traxler, M. F., López, D., and Kolter, R. (2011) Antibiotics as signal molecules. Chem. Rev. 111, 5492-5505
66. Johnson, C. L., Pechonick, E., Park, S. D., Havemann, G. D., Leal, N. A., and Bobik T. A. (2001) Functional genomic, biochemical, and genetic characterization of the Salmonella pduO gene, an ATP:Cob(I)alamin adenosyltransferase gene. J. Bacteriol. 183, 1577-1584
67. Sun, J., van den Heuvel, J., Soucaille, P., Qu, Y., and Zeng, A. P. (2003) Comparative genomic analysis of dha regulon and related genes for anaerobic glycerol metabolism in bacteria. Biotechnol. Prog. 19, 263-272
68. Parsons, J. B., Lawrence, A. D., McLean, K. J., Munro, A. W., Rigby, S. E., and Warren, M. J. (2010) Characterisation of PduS, the pdu metabolosome corrin reductase, and evidence of substructural organisation within the bacterial microcompartment. PLoS One 5, e14009
69. Margraf, T., Schenk, G., and Torda, A. E. (2009) The SALAMI protein structure server. Nucleic Acids Res. 37, W480-W484