A heme-based redox sensor in the methanogenic archaeon methanosarcina acetivorans

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 18458-18472

  Molitor, Bastian ^a   Stassen, Marc ^a   Modi, Anuja ^b   El Mashtoly, Samir F ^c   Laurich, Christoph ^d   Lubitz, Wolfgang ^d   Dawson, John H ^b   Rother, Michael ^a,e   Frankenberg Dinkel, Nicole ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COVALENTLY BOUND; ENVIRONMENTAL STIMULI; HEME COFACTOR; KINASE ACTIVITY; METHANOSARCINA ACETIVORANS; MULTI DOMAINS; RECEPTIVE PROCESS; REDOX-ACTIVE;

ENZYMES; MICROORGANISMS; SIGNAL TRANSDUCTION;

PORPHYRINS;

CARBON MONOXIDE; CORRINOID; CYSTEINE; DIMETHYL SULFIDE; HEME; HYBRID PROTEIN; IMIDAZOLE; ISOPROTEIN; METHYLTRANSFERASE; PHOSPHOTRANSFERASE; PROTEIN MA4561; TETRAPYRROLE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; BACTERIUM MUTANT; BIOSENSOR; CHROMATOPHORE; CONTROLLED STUDY; COVALENT BOND; CYTOPLASM; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; LIGAND BINDING; METABOLISM; METHANOSARCINA ACETIVORANS; NONHUMAN; OXIDATION REDUCTION REACTION; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

ARCHAEA; HEME; METHANOSARCINA; RAMAN SPECTROSCOPY; REDOX SIGNALING; SENSOR KINASE; SIGNAL TRANSDUCTION; UV SPECTROSCOPY;

ARCHAEAL PROTEINS; BINDING SITES; BLOTTING, WESTERN; HEME; METHANE; METHANOSARCINA; METHYLTRANSFERASES; MODELS, MOLECULAR; MUTATION; OXIDATION-REDUCTION; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SPECTRUM ANALYSIS, RAMAN; SULFIDES;

EID: 84880053915     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.476267     Document Type: Article

References (67)

1. Green, J., Crack, J. C., Thomson, A. J., and LeBrun, N. E. (2009) Bacterial sensors of oxygen. Curr. Opin. Microbiol. 12, 145-151
2. Hou, S., Larsen, R. W., Boudko, D., Riley, C. W., Karatan, E., Zimmer, M., Ordal, G. W., and Alam, M. (2000) Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540-544 (Pubitemid 30082198)
3. Boon, E. M., and Marletta, M. A. (2005) Ligand specificity of H-NOX domains: From sGC to bacterial NO sensors. J. Inorg. Biochem. 99, 892-902 (Pubitemid 40461919)
4. Poulos, T. L. (2006) Soluble guanylate cyclase. Curr. Opin. Struct. Biol. 16, 736-743 (Pubitemid 44834471)
5. Moskvin, O. V., Kaplan, S., Gilles-Gonzalez, M. A., and Gomelsky, M. (2007) Novel heme-based oxygen sensor with a revealing evolutionary history. J. Biol. Chem. 282, 28740-28748 (Pubitemid 47606067)
6. Aono, S., Nakajima, H., Saito, K., and Okada, M. (1996) A novel heme protein that acts as a carbon monoxide-dependent transcriptional activator in Rhodospirillum rubrum. Biochem. Biophys. Res. Commun. 228, 752-756 (Pubitemid 26421450)
7. Gilles-Gonzalez, M. A., and Gonzalez, G. (2004) Signal transduction by heme-containing PAS-domain proteins. J. Appl. Physiol. 96, 774-783 (Pubitemid 38140186)
8. Gilles-Gonzalez, M. A., and Gonzalez, G. (1993) Regulation of the kinase activity of heme protein FixL from the two-component system FixL/ FixJ of Rhizobium meliloti. J. Biol. Chem. 268, 16293-16297 (Pubitemid 23229929)
9. Delgado-Nixon, V. M., Gonzalez, G., and Gilles-Gonzalez, M. A. (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39, 2685-2691 (Pubitemid 30148922)
10. Chang, A. L., Tuckerman, J. R., Gonzalez, G., Mayer, R., Weinhouse, H., Volman, G., Amikam, D., Benziman, M., and Gilles-Gonzalez, M. A. (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40, 3420-3426 (Pubitemid 32242798)
11. Ioanoviciu, A., Yukl, E. T., Moënne-Loccoz, P., and de Montellano, P. R. (2007) DevS, a heme-containing two-component oxygen sensor of Mycobacterium tuberculosis. Biochemistry 46, 4250-4260 (Pubitemid 46559392)
12. Kumar, A., Toledo, J. C., Patel, R. P., Lancaster, J. R., Jr., and Steyn, A. J. (2007) Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl. Acad. Sci. U.S.A. 104, 11568-11573 (Pubitemid 47175053)
13. Dolla, A., Fu, R., Brumlik, M. J., and Voordouw, G. (1992) Nucleotide sequence of dcrA, a Desulfovibrio vulgaris Hildenborough chemoreceptor gene, and its expression in Escherichia coli. J. Bacteriol. 174, 1726-1733
14. Fu, R., Wall, J. D., and Voordouw, G. (1994) DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment. J. Bacteriol. 176, 344-350 (Pubitemid 24034051)
15. Yoshioka, S., Kobayashi, K., Yoshimura, H., Uchida, T., Kitagawa, T., and Aono, S. (2005) Biophysical properties of a c-type heme in chemotaxis signal transducer protein DcrA. Biochemistry 44, 15406-15413 (Pubitemid 41683135)
16. Tuckerman, J. R., Gonzalez, G., Sousa, E. H., Wan, X., Saito, J. A., Alam, M., and Gilles-Gonzalez, M. A. (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48, 9764-9774
17. Sasakura, Y., Yoshimura-Suzuki, T., Kurokawa, H., and Shimizu, T. (2006) Structure-function relationships of EcDOS, a heme-regulated phosphodiesterase from Escherichia coli. Acc. Chem. Res. 39, 37-43
18. Masuda, S., and Bauer, C. E. (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110, 613-623 (Pubitemid 35247841)
19. Sousa, E. H., Tuckerman, J. R., Gonzalez, G., and Gilles-Gonzalez, M. A. (2007) DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Protein Sci. 16, 1708-1719 (Pubitemid 47195697)
20. Kitanishi, K., Kobayashi, K., Uchida, T., Ishimori, K., Igarashi, J., and Shimizu, T. (2011) Identification and functional and spectral characterization of a globin-coupled histidine kinase from Anaeromyxobacter sp. Fw109-5. J. Biol. Chem. 286, 35522-35534
21. Ulrich, L. E., Koonin, E. V., and Zhulin, I. B. (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13, 52-56 (Pubitemid 40174862)
22. Ashby, M. K. (2006) Distribution, structure and diversity of "bacterial" genes encoding two-component proteins in the Euryarchaeota. Archaea 2, 11-30 (Pubitemid 44377984)
23. Koretke, K. K., Lupas, A. N., Warren, P. V., Rosenberg, M., and Brown, J. R. (2000) Evolution of two-component signal transduction. Mol. Biol. Evol. 17, 1956-1970
24. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction. Annu. Rev. Biochem. 69, 183-215
25. Galperin, M. Y. (2010) Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol. 13, 150-159
26. Karniol, B., Wagner, J. R., Walker, J. M., and Vierstra, R. D. (2005) Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem. J. 392, 103-116 (Pubitemid 41689406)
27. Guss, A. M., Rother, M., Zhang, J. K., Kulkarni, G., and Metcalf, W. W. (2008) New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species. Archaea 2, 193-203
28. Metcalf, W. W., Zhang, J. K., Apolinario, E., Sowers, K. R., and Wolfe, R. S. (1997) A genetic system for Archaea of the genus Methanosarcina: Liposome-mediated transformation and construction of shuttle vectors. Proc. Natl. Acad. Sci. U.S.A. 94, 2626-2631
29. Metcalf, W. W., Zhang, J. K., Shi, X., and Wolfe, R. S. (1996) Molecular, genetic, and biochemical characterization of the serC gene of Methanosarcina barkeri Fusaro. J. Bacteriol. 178, 5797-5802 (Pubitemid 26327686)
30. Boccazzi, P., Zhang, J. K., and Metcalf, W. W. (2000) Generation of dominant selectable markers for resistance to pseudomonic acid by cloning and mutagenesis of the ileS gene from the archaeon Methanosarcina barkeri Fusaro. J. Bacteriol. 182, 2611-2618 (Pubitemid 30212923)
31. Vargas, C., McEwan, A. G., and Downie, J. A. (1993) Detection of c-type cytochromes using enhanced chemiluminescence. Anal. Biochem. 209, 323-326 (Pubitemid 23130193)
32. Teale, F. W. (1959) Cleavage of the haem-protein link by acid methylethylketone. Biochim. Biophys. Acta 35, 543
33. Berry, E. A., and Trumpower, B. L. (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal. Biochem. 161, 1-15
34. Huff, A. M., Chang, C. K., Cooper, D. K., Smith, K. M., and Dawson, J. H. (1993) Imidazole-and alkylamine-ligated iron(II,III) chlorin complexes as models for histidine and lysine coordination to iron in dihydroporphyrincontaining proteins: Characterization with magnetic circular dichroism spectroscopy. Inorg. Chem. 32, 1460-1466
35. Pritchett, M. A., Zhang, J. K., and Metcalf, W. W. (2004) Development of a markerless genetic exchange method for Methanosarcina acetivorans C2A and its use in construction of new genetic tools for methanogenic archaea. Appl. Environ. Microbiol. 70, 1425-1433 (Pubitemid 38365122)
36. Daltrop, O., Allen, J. W., Willis, A. C., and Ferguson, S. J. (2002) In vitro formation of a c-type cytochrome. Proc. Natl. Acad. Sci. U.S.A. 99, 7872-7876 (Pubitemid 34650972)
37. Pipirou, Z., Bottrill, A. R., Svistunenko, D. A., Efimov, I., Basran, J., Mistry, S. C., Cooper, C. E., and Raven, E. L. (2007) The reactivity of heme in biological systems: Autocatalytic formation of both tyrosine-heme and tryptophan-heme covalent links in a single protein architecture. Biochemistry 46, 13269-13278 (Pubitemid 350136368)
38. Tomlinson, E. J., and Ferguson, S. J. (2000) Loss of either of the two hemebinding cysteines from a class I c-type cytochrome has a surprisingly small effect on physicochemical properties. J. Biol. Chem. 275, 32530-32534
39. Daltrop, O., Smith, K. M., and Ferguson, S. J. (2003) Stereoselective in vitro formation of c-type cytochrome variants from Hydrogenobacter thermophilus containing only a single thioether bond. J. Biol. Chem. 278, 24308-24313 (Pubitemid 37548581)
40. Pipirou, Z., Bottrill, A. R., Metcalfe, C. M., Mistry, S. C., Badyal, S. K., Rawlings, B. J., and Raven, E. L. (2007) Autocatalytic formation of a covalent link between tryptophan 41 and the heme in ascorbate peroxidase. Biochemistry 46, 2174-2180 (Pubitemid 46355326)
41. Kuzelová, K., Mrhalová, M., and Hrkal, Z. (1997) Kinetics of heme interaction with heme-binding proteins: The effect of heme aggregation state. Biochim. Biophys. Acta 1336, 497-501 (Pubitemid 27467051)
42. Abe, M., Kitagawa, T., and Kyogoku, Y. (1978) Resonance Raman spectra of octaethylporphyrinato-Ni(II) and meso-deuterated and 15Nsubstituted derivatives. II. A normal coordinate analysis. J. Chem. Phys. 69, 4526-4534
43. El-Mashtoly, S. F., Takahashi, H., Kurokawa, H., Sato, A., Shimizu, T., and Kitagawa, T. (2008) Resonance Raman investigation of redox-induced structural changes of protein and heme in the sensor domain of EcDOS protein. J. Raman Spectrosc. 39, 1614-1626
44. Li, X. Y., and Spiro, T. G. (1988) Is bound carbonyl linear or bent in heme proteins? Evidence from resonance Raman and infrared spectroscopic data. J. Am. Chem. Soc. 110, 6024-6033
45. Spiro, T. G., Stong, J. D., and Stein, P. (1979) Porphyrin core expansion and doming in heme proteins. New evidence from resonance Raman spectra of six-coordinate high-spin iron(III) hemes. J. Am. Chem. Soc. 101, 2648-2655
46. Du, J., Sono, M., and Dawson, J. H. (2011) Ferric His93Gly myoglobin cavity mutant and its complexes with thioether and selenolate as heme protein models. J. Porphyr. Phthalocyanines 15, 29-38
47. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protoc. 4, 363-371
48. Wass, M. N., Kelley, L. A., and Sternberg, M. J. (2010) 3DLigandSite: Predicting ligand-binding sites using similar structures. Nucleic Acids Res. 38, W469-W473
49. Ikeuchi, M., and Ishizuka, T. (2008) Cyanobacteriochromes: A new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 7, 1159-1167
50. Kranz, R. G., Richard-Fogal, C., Taylor, J. S., and Frawley, E. R. (2009) Cytochrome c biogenesis: Mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol. Mol. Biol. Rev. 73, 510-528
51. Thöny-Meyer, L. (2002) Cytochrome c maturation: A complex pathway for a simple task? Biochem. Soc. Trans. 30, 633-638 (Pubitemid 35001614)
52. Aono, S., Kato, T., Matsuki, M., Nakajima, H., Ohta, T., Uchida, T., and Kitagawa, T. (2002) Resonance Raman and ligand binding studies of the oxygen-sensing signal transducer protein HemAT from Bacillus subtilis. J. Biol. Chem. 277, 13528-13538 (Pubitemid 34975647)
53. Tanaka, A., and Shimizu, T. (2008) Ligand binding to the Fe(III)-protoporphyrin IX complex of phosphodiesterase from Escherichia coli (Ec DOS) markedly enhances catalysis of cyclic di-GMP: Roles of Met95, Arg97, and Phe113 of the putative heme distal side in catalytic regulation and ligand binding. Biochemistry 47, 13438-13446
54. Tanaka, A., Takahashi, H., and Shimizu, T. (2007) Critical role of the heme axial ligand, Met95, in locking catalysis of the phosphodiesterase from Escherichia coli (Ec DOS) toward cyclic diGMP. J. Biol. Chem. 282, 21301-21307 (Pubitemid 47099927)
55. Duff, S. M., Wittenberg, J. B., and Hill, R. D. (1997) Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands. J. Biol. Chem. 272, 16746-16752 (Pubitemid 27289769)
56. Shelver, D., Kerby, R. L., He, Y., and Roberts, G. P. (1997) CooA, a COsensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein. Proc. Natl. Acad. Sci. U.S.A. 94, 11216-11220 (Pubitemid 27450978)
57. Kitanishi, K., Kobayashi, K., Kawamura, Y., Ishigami, I., Ogura, T., Nakajima, K., Igarashi, J., Tanaka, A., and Shimizu, T. (2010) Important roles of Tyr43 at the putative heme distal side in the oxygen recognition and stability of the Fe(II)-O2 complex of YddV, a globin-coupled heme-based oxygen sensor diguanylate cyclase. Biochemistry 49, 10381-10393
58. Gilles-Gonzalez, M. A., Gonzalez, G., Perutz, M. F., Kiger, L., Marden, M. C., and Poyart, C. (1994) Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochemistry 33, 8067-8073 (Pubitemid 24223828)
59. Galagan, J. E., Nusbaum, C., Roy, A., Endrizzi, M. G., Macdonald, P., FitzHugh, W., Calvo, S., Engels, R., Smirnov, S., Atnoor, D., Brown, A., Allen, N., Naylor, J., Stange-Thomann, N., DeArellano, K., Johnson, R., Linton, L., McEwan, P., McKernan, K., Talamas, J., Tirrell, A., Ye, W., Zimmer, A., Barber, R. D., Cann, I., Graham, D. E., Grahame, D. A., Guss, A. M., Hedderich, R., Ingram-Smith, C., Kuettner, H. C., Krzycki, J. A., Leigh, J. A., Li, W., Liu, J., Mukhopadhyay, B., Reeve, J. N., Smith, K., Springer, T. A., Umayam, L. A., White, O., White, R. H., Conway de Macario, E., Ferry, J. G., Jarrell, K. F., Jing, H., Macario, A. J., Paulsen, I., Pritchett, M., Sowers, K. R., Swanson, R. V., Zinder, S. H., Lander, E., Metcalf, W. W., and Birren, B. (2002) The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res. 12, 532-542 (Pubitemid 34308633)
60. Moran, J. J., House, C. H., Freeman, K. H., and Ferry, J. G. (2005) Trace methane oxidation studied in several Euryarchaeota under diverse conditions. Archaea 1, 303-309 (Pubitemid 40801837)
61. Tietze, M., Beuchle, A., Lamla, I., Orth, N., Dehler, M., Greiner, G., and Beifuss, U. (2003) Redox potentials of methanophenazine and CoB-S-SCoM, factors involved in electron transport in methanogenic archaea. Chembiochem 4, 333-335 (Pubitemid 36505202)
62. Bose, A., Kulkarni, G., and Metcalf, W. W. (2009) Regulation of putative methyl-sulphide methyltransferases in Methanosarcina acetivorans C2A. Mol. Microbiol. 74, 227-238
63. Oelgeschläger, E., and Rother, M. (2009) In vivo role of three fused corrinoid/ methyl transfer proteins in Methanosarcina acetivorans. Mol. Microbiol. 72, 1260-1272
64. Moran, J. J., House, C. H., Vrentas, J. M., and Freeman, K. H. (2008) Methyl sulfide production by a novel carbon monoxide metabolism in Methanosarcina acetivorans. Appl. Environ. Microbiol. 74, 540-542
65. Bose, A., and Metcalf, W. W. (2008) Distinct regulators control the expression of methanol methyltransferase isozymes in Methanosarcina acetivorans C2A. Mol. Microbiol. 67, 649-661
66. Dawson, J. H., Kadkhodayan, S., Zhuang, C., and Sono, M. (1992) On the use of iron octa-alkylporphyrins as models for protoporphyrin IX-containing heme systems in studies employing magnetic circular dichroism spectroscopy. J. Inorg. Biochem. 45, 179-192
67. Cheek, J., Mandelman, D., Poulos, T. L., and Dawson, J. H. (1999) A study of the K+-site mutant of ascorbate peroxidase: Mutations of protein residues on the proximal side of the heme cause changes in iron ligation on the distal side. J. Biol. Inorg. Chem. 4, 64-72 (Pubitemid 29113814)