Native electrospray mass spectrometry reveals the nature and stoichiometry of pigments in the FMO photosynthetic antenna protein

Biochemistry

Volumn 50, Issue 17, 2011, Pages 3502-3511

  Wen, Jianzhong ^a   Zhang, Hao ^a   Gross, Michael L ^a   Blankenship, Robert E ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTENNA COMPLEXES; ANTENNA PROTEINS; BACTERIOCHLOROPHYLLS; DIRECT MASS SPECTROMETRY; ELECTROSPRAY MASS SPECTROMETRY; HPLC ANALYSIS; MASS ANALYSIS; MASS SPECTRA; MOLECULAR MECHANISM; PROTEIN COMPLEXES; SPECTRAL FEATURE; STRUCTURAL MODELS;

ANTENNAS; CHLOROPHYLL; ENERGY TRANSFER; MAMMALS; MASS SPECTROMETRY; MODEL STRUCTURES; OLIGOMERS; STOICHIOMETRY;

PROTEINS;

BACTERIOCHLOROPHYLL A; PIGMENT; PROTEIN FMO; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ANTENNA; ARTICLE; COMPLEX FORMATION; ELECTROSPRAY MASS SPECTROMETRY; ENERGY TRANSFER; MOLECULAR WEIGHT; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; STOICHIOMETRY;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLL A; CHLOROBI; LIGHT-HARVESTING PROTEIN COMPLEXES; MODELS, MOLECULAR; MOLECULAR WEIGHT; MULTIPROTEIN COMPLEXES; PIGMENTS, BIOLOGICAL; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 79955412076     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200239k     Document Type: Article

References (57)

1. Lewis, N. S. (2007) Toward cost-effective solar energy use Science 315, 798-801
2. Barber, J. (2009) Photosynthetic energy conversion: natural and artificial Chem. Soc. Rev. 38, 185-196
3. Hambourger, M., Moore, G. F., Kramer, D. M., Gust, D., Moore, A. L., and Moore, T. A. (2009) Biology and technology for photochemical fuel production Chem. Soc. Rev. 38, 25-35
4. Nocera, D. G. (2009) Personalized energy: the home as a solar power station and solar gas station ChemSusChem 2, 387-390
5. Li, Y. F., Zhou, W., Blankenship, R. E., and Allen, J. P. (1997) Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum J. Mol. Biol. 271, 456-471 (Pubitemid 27348510)
6. Tronrud, D. E., Schmid, M. F., and Matthews, B. W. (1986) Structure and X-Ray amino acid sequence of a bacteriochlorophyll a protein from Prosthecochloris aestuarii refined at 1.9 A resolution J. Mol. Biol. 188, 443-454
7. Fenna, R. E. and Matthews, B. W. (1975) Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola Nature 258, 573-577
8. Tronrud, D. E., Wen, J., Gay, L., and Blankenship, R. E. (2009) The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria Photosynth. Res. 100, 79-87
9. Tsukatani, Y., Wen, J., Blankenship, R. E., and Bryant, D. A. (2010) Characterization of the FMO protein from the aerobic chlorophototroph, Candidatus Chloracidobacterium thermophilum Photosynth. Res. 104, 201-209
10. Wen, J., Harada, J., Buyle, K., Yuan, K., Tamiaki, H., Oh-Oka, H., Loomis, R. A., and Blankenship, R. E. (2010) Characterization of an FMO variant of Chlorobaculum tepidum carrying bacteriochlorophyll a esterified by geranylgeraniol Biochemistry 49, 5455-5463
11. Larson, C. R., Seng, C., Lauman, L., Matthies, H. J., Wen, J., Blankenship, R. E., and Allen, J. P. (2010) The three dimensional structure of the FMO protein from Pelodictyon phaeum and the implications for energy transfer Photosynth. Res. 107, 139-150
12. Brixner, T., Stenger, J., Vaswani, H. M., Cho, M., Blankenship, R. E., and Fleming, G. R. (2005) Two-dimensional spectroscopy of electronic couplings in photosynthesis Nature 434, 625-628 (Pubitemid 40488551)
13. Cheng, Y. C. and Fleming, G. R. (2009) Dynamics of light harvesting in photosynthesis Annu. Rev. Phys. Chem. 60, 241-262
14. Engel, G. S., Calhoun, T. R., Read, E. L., Ahn, T. K., Mancal, T., Cheng, Y. C., Blankenship, R. E., and Fleming, G. R. (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems Nature 446, 782-786 (Pubitemid 46582029)
15. Panitchayangkoon, G., Hayes, D., Fransted, K. A., Caram, J. R., Harel, E., Wen, J., Blankenship, R. E., and Engel, G. S. (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature Proc. Natl. Acad. Sci. U.S.A. 107, 12766-12770
16. Savikhin, S., Zhou, W., Blankenship, R. E., and Struve, W. S. (1994) Femtosecond energy transfer and spectral equilibration in bacteriochlorophyll a protein antenna trimers from the green bacterium Chlorobium tepidum Biophys. J. 66, 110-113 (Pubitemid 24016490)
17. Adolphs, J. and Renger, T. (2006) How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria Biophys. J. 91, 2778-2797 (Pubitemid 44526469)
18. Louwe, R., Vrieze, J., Hoff, A., and T., A. (1997) Toward an integral interpretation of the optical steady-state spectra of the FMO-complex of Prosthecochloris aestuarii. 2. exciton simulations J. Phys. Chem. B 101, 11280-11287 (Pubitemid 127627986)
19. Pearlstein, R. (1992) Theory of the optical spctra of the bacteriochlorophyll a antenna protein trimer from Prosthecochloris aestuarii Photosynth. Res. 31, 213-226
20. Renger, T. (2009) Theory of excitation energy transfer: from structure to function Photosynth. Res. 102, 471-485
21. Milder, M. T., Bruggemann, B., van Grondelle, R., and Herek, J. L. (2010) Revisiting the optical properties of the FMO protein Photosynth. Res. 104, 257-274
22. Blankenship, R. E. (2003) Molecular Mechanisms of Photosynthesis, Blackwell Science, Oxford, UK.
23. Olson, J. M. (2004) The FMO protein Photosynth. Res. 80, 181-187 (Pubitemid 38889626)
24. Bryant, D. A., Costas, A. M., Maresca, J. A., Chew, A. G., Klatt, C. G., Bateson, M. M., Tallon, L. J., Hostetler, J., Nelson, W. C., Heidelberg, J. F., and Ward, D. M. (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium Science 317, 523-526 (Pubitemid 47196118)
25. Wen, J., Tsukatani, Y., Cui, W., Zhang, H., Gross, M. L., Bryant, D. A., and Blankenship, R. E. (2010) Structural model and spectroscopic characteristics of the FMO antenna protein from the aerobic chlorophototroph, Candidatus Chloracidobacterium thermophilum Biochim. Biophys. Acta 1807, 157-164
26. Müh, F., Madjet, M. E. A., Adolphs, J., Abdurahman, A., Rabenstein, B., Ishikita, H., Knapp, E. W., and Renger, T. (2007) alpha-Helices direct excitation energy flow in the Fenna-Matthews-Olson protein Proc. Natl. Acad. Sci. U.S.A. 104, 16862-16867 (Pubitemid 350210956)
27. Wen, J., Zhang, H., Gross, M. L., and Blankenship, R. E. (2009) Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting Proc. Natl. Acad. Sci. U.S.A. 106, 6134-6139
28. Nagy, A., Prokhorenko, V., and Miller, R. J. (2006) Do we live in a quantum world? Advances in multidimensional coherent spectroscopies refine our understanding of quantum coherences and structural dynamics of biological systems Curr. Opin. Struct. Biol. 16, 654-663 (Pubitemid 44466413)
29. Read, E. L., Schlau-Cohen, G. S., Engel, G. S., Wen, J. Z., Blankenship, R. E., and Fleming, G. R. (2008) Visualization of excitonic structure in the Fenna-Matthews-Olson photosynthetic complex by polarization-dependent two-dimensional electronic spectroscopy Biophys. J. 95, 847-856
30. Abramavicius, D., Voronine, D. V., and Mukamel, S. (2008) Double-quantum resonances and exciton-scattering in coherent 2D spectroscopy of photosynthetic complexes Proc. Natl. Acad. Sci. U.S.A. 105, 8525-8530 (Pubitemid 351987713)
31. Ishizaki, A. and Fleming, G. R. (2009) Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature Proc. Natl. Acad. Sci. U.S.A. 106, 17255-17260
32. Rebentrost, P., Mohseni, M., and Aspuru-Guzik, A. (2009) Role of quantum coherence and environmental fluctuations in chromophoric energy transport J. Phys. Chem. B 113, 9942-9947
33. Sarovar, M., Ishizaki, A., Fleming, G. R., and Whaley, K. B. (2010) Quantum entanglement in photosynthetic light-harvesting complexes Nature Phys. 6, 462-467
34. Ben-Shem, A., Frolow, F., and Nelson, N. (2004) Evolution of photosystem I-from symmetry through pseudosymmetry to asymmetry FEBS Lett. 564, 274-280 (Pubitemid 38520933)
35. Liu, T., Belov, M. E., Jaitly, N., Qian, W. J., and Smith, R. D. (2007) Accurate mass measurements in proteomics Chem. Rev. 107, 3621-3653 (Pubitemid 47322746)
36. Lu, B., Xu, T., Park, S. K., and Yates, J. R., 3rd. (2009) Shotgun protein identification and quantification by mass spectrometry Methods Mol. Biol. 564, 261-288
37. Yates, J. R., Ruse, C. I., and Nakorchevsky, A. (2009) Proteomics by mass spectrometry: approaches, advances, and applications Annu. Rev. Biomed. Eng. 11, 49-79
38. Heck, A. J. and Van Den Heuvel, R. H. (2004) Investigation of intact protein complexes by mass spectrometry Mass Spectrom. Rev. 23, 368-389
39. Hernandez, H. and Robinson, C. V. (2007) Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry Nature Protoc. 2, 715-726 (Pubitemid 47040033)
40. Loo, J. A. (2000) Electrospray ionization mass spectrometry: a technology for studying noncovalent macromolecular complexes Int. J. Mass Spectrom. 200, 175-186 (Pubitemid 32015921)
41. Sobott, F. and Robinson, C. V. (2002) Protein complexes gain momentum Curr. Opin. Struct. Biol. 12, 729-734 (Pubitemid 36009488)
42. Franken, E. M. and Amesz, J. (1997) Electron transport and triplet formation in membrane fragments of the green sulfur bacterium Prosthecochloris aestuarii Biochim. Biophys. Acta 1319, 214-222 (Pubitemid 27156892)
43. Wahlund, T. M., Woese, C. R., Castenholz, R. W., and Madigan, M. T. (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov Arch. Microbiol. 156, 81-90
44. Zhang, H., Cui, W., Wen, J., Blankenship, R. E., and Gross, M. L. (2010) Native electrospray and electron-capture dissociation in FTICR mass spectrometry provide top-down sequencing of a protein component in an intact protein assembly J. Am. Soc. Mass Spectrom. 21, 1966-1968
45. Addlesee, H. A. and Hunter, C. N. (1999) Physical mapping and functional assignment of the geranylgeranyl-bacteriochlorophyll reductase gene, bchP, of Rhodobacter sphaeroides J. Bacteriol. 181, 7248-7255
46. Bollivar, D. W., Wang, S., Allen, J. P., and Bauer, C. E. (1994) Molecular genetic analysis of terminal steps in bacteriochlorophyll a biosynthesis: characterization of a Rhodobacter capsulatus strain that synthesizes geranylgeraniol-esterified bacteriochlorophyll a Biochemistry 33, 12763-12768 (Pubitemid 24352865)
47. Frigaard, N. U., Voigt, G. D., and Bryant, D. A. (2002) Chlorobium tepidum mutant lacking bacteriochlorophyll c made by inactivation of the bchK gene, encoding bacteriochlorophyll c synthase J. Bacteriol. 184, 3368-3376 (Pubitemid 34568947)
48. Liepold, L., Oltrogge, L. M., Suci, P. A., Young, M. J., and Douglas, T. (2009) Correct charge state assignment of native electrospray spectra of protein complexes J. Am. Soc. Mass Spectrom. 20, 435-442
49. McKay, A. R., Ruotolo, B. T., Ilag, L. L., and Robinson, C. V. (2006) Mass measurements of increased accuracy resolve heterogeneous populations of intact ribosomes J. Am. Chem. Soc. 128, 11433-11442 (Pubitemid 44338835)
50. Van Berkel, G. J., McLuckey, S. A., and Glish, G. L. (1991) Electrospray ionization of porphyrins using a quadrupole ion trap for mass analysis Anal. Chem. 63, 1098-1109
51. Verzegnassi, L., Riffe-Chalard, C., and Gulacar, F. O. (2000) Rapid identification of Mg-chelated chlorins by on-line high performance liquid chromatography/atmospheric pressure chemical ionization mass spectrometry Rapid Commun. Mass Spectrom. 14, 590-594 (Pubitemid 30170361)
52. Breuker, K. and McLafferty, F. W. (2008) Stepwise evolution of protein native structure with electrospray into the gas phase, 10(-12) to 10(2) s Proc. Natl. Acad. Sci. U.S.A. 105, 18145-18152
53. Weinmann, W., Stoertzel, M., Vogt, S., and Wendt, J. (2001) Tune compounds for electrospray ionisation/in-source collision-induced dissociation with mass spectral library searching J. Chromatogr., A 926, 199-209 (Pubitemid 32739019)
54. Melkozernov, A. N., Olson, J. M., Li, Y. F., Allen, J. P., and Blankenship, R. E. (1998) Orientation and excitonic interactions of the Fenna-Matthews-Olson Protein in membranes of the green sulfur bacterium Chlorobium tepidum Photosynth. Res. 56, 315-328 (Pubitemid 28403755)
55. Schmidt am Busch, Müh, F., Mudget, M. E.-A., and Renger, T. (2011) The eighth bacteriochlorophyll completes the excitation energy funnel in the FMO Protein J. Phys. Chem. Lett. 2, 93-98
56. Pedersen, M. O., Borch, J., Hojrup, P., Cox, R. P., and Miller, M. (2006) The light-harvesting antenna of Chlorobium tepidum: interactions between the FMO protein and the major chlorosome protein CsmA studied by surface plasmon resonance Photosynth. Res. 89, 63-69 (Pubitemid 44440484)
57. Pedersen, M. O., Linnanto, J., Frigaard, N. U., Nielsen, N. C., and Miller, M. (2010) A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic green bacteria Photosynth. Res. 104, 233-243