High throughput engineering to revitalize a vestigial electron transfer pathway in bacterial photosynthetic reaction centers

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8507-8514

  Faries, Kaitlyn M ^a   Kressel, Lucas L ^b   Wander, Marc J ^b   Holten, Dewey ^a   Laible, Philip D ^b   Kirmaier, Christine ^a   Hanson, Deborah K ^b  

^a WASHINGTON UNIVERSITY   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PHOTOSYNTHETIC REACTION; BACTERIAL REACTION; BIO-INSPIRED; CHARGE SEPARATIONS; CHARGE STABILIZATION; CHEMICAL ENERGY; COFACTORS; EFFICIENT CONSTRUCTION; ELECTRON TRANSFER; ELECTRON TRANSFER PATHWAYS; ENERGETIC FACTORS; HIGH THROUGHPUT; LIGHT ENERGY; MOLECULAR EVOLUTION; MULTIPLE SUBSTITUTIONS; PHOTOSYNTHETIC REACTION CENTER; REACTION CENTER; SEQUENCE SIMILARITY; SITE-SPECIFIC MUTAGENESIS; STRUCTURE-FUNCTION RELATIONSHIP; TRANS-MEMBRANE PROTEINS; TRANSMEMBRANE ELECTRON TRANSFER; TRANSMEMBRANES;

DIAGNOSIS; MUTAGENESIS; PHOTOSYNTHESIS; SEPARATION; THROUGHPUT;

ELECTRON TRANSITIONS;

QUINONE DERIVATIVE;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM MUTANT; CISTRON; CONTROLLED STUDY; ELECTRON TRANSPORT; MUTAGENESIS; NONHUMAN; PHOTOSYNTHETIC REACTION CENTER; PRIORITY JOURNAL; PROTEIN PURIFICATION; RHODOBACTER CAPSULATUS; SEQUENCE HOMOLOGY; SPECTROSCOPY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ELECTRON TRANSPORT; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN ENGINEERING; RHODOCOCCUS;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 84858054802     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.326447     Document Type: Article

References (58)

1. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. C. (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc. Natl. Acad. Sci. U.S.A. 84, 5730-5734
2. Chang, C. H., el-Kabbani, O., Tiede, D., Norris, J., and Schiffer, M. (1991) Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 30, 5352-5360
3. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985) Structure of the protein subunits in the photosynthetic reaction center from Rhodopseudomonas viridis at 3 Å resolution. Nature 318, 618-624 (Pubitemid 16172409)
4. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 A resolution: cofactors and protein-cofactor interactions. Structure 2, 925-936
5. Dashdorj, N., Xu, W., Cohen, R. O., Golbeck, J. H., and Savikhin, S. (2005) Asymmetric electron transfer in cyanobacterial photosystem I: charge separation and secondary electron transfer dynamics of mutations near the primary electron acceptor A0. Biophys. J. 88, 1238-1249 (Pubitemid 40975951)
6. Guergova-Kuras, M., Boudreaux, B., Joliot, A., Joliot, P., and Redding, K. (2001) Evidence for two active branches for electron transfer in photosystem I. Proc. Natl. Acad. Sci. U.S.A. 98, 4437-4442 (Pubitemid 32294995)
7. Joliot, P., and Joliot, A. (1999) In vivo analysis of the electron transfer within photosystem I: are the two phylloquinones involved? Biochemistry 38, 11130-11136
8. Ramesh, V. M., Gibasiewicz, K., Lin, S., Bingham, S. E., and Webber, A. N. (2004) Bidirectional electron transfer in photosystem I: accumulation of A0- in A-side or B-side mutants of the axial ligand to chlorophyll A0. Biochemistry 43, 1369-1375 (Pubitemid 38176536)
9. Wakeham, M. C., and Jones, M. R. (2005) Rewiring photosynthesis: engineering wrong-way electron transfer in the purple bacterial reaction centre. Biochem. Soc. Trans. 33, 851-857 (Pubitemid 41160878)
10. Bylina, E. J., Kirmaier, C., McDowell, L., Holten, D., and Youvan, D. C. (1988) Influence of an amino-acid residue on the optical properties and electron transfer dynamics of a photosynthetic reaction centre complex. Nature 336, 182-184
11. DiMagno, T. L., PD, Reddy, N. R., Small, G. J., Norris, J. R., Schiffer, M., and Hanson, D. K. (1998) Protein-chromophore interactions: spectral shifts report the consequences of mutations in the bacterial photosynthetic reaction center. Spectrochim. Acta Part A 54, 1247-1267
12. Heller, B. A., Holten, D., and Kirmaier, C. (1996) Effects of Asp residues near the L-side pigments in bacterial reaction centers. Biochemistry 35, 15418-15427 (Pubitemid 26408878)
13. Katilius, E., Babendure, J. L., Katiliene, Z., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (2003) Manipulations of the B-side charge-separated states' energetics in the Rhodobacter sphaeroides reaction center. J. Phys. Chem. 107, 12029-12034
14. Williams, J. C., Alden, R. G., Murchison, H. A., Peloquin, J. M., Woodbury, N. W., and Allen, J. P. (1992) Effects of mutations near the bacteriochlorophylls in reaction centers from Rhodobacter sphaeroides. Biochemistry 31, 11029-11037
15. Allen, J. P., and Williams, J. C. (1995) Relationship between the oxidation potential of the bacteriochlorophyll dimer and electron transfer in photosynthetic reaction centers. J. Bioenerg. Biomembr. 27, 275-283
16. de Boer, A. L., Neerken, S., de Wijn, R., Permentier, H. P., Gast, P., Vijgenboom, E., and Hoff, A. J. (2002) B-branch electron transfer in reaction centers of Rhodobacter sphaeroides assessed with site-directed mutagenesis. Photosynth. Res. 71, 221-239 (Pubitemid 34635234)
17. Heller, B. A., Holten, D., and Kirmaier, C. (1995) Control of electron transfer between the L- and M-sides of photosynthetic reaction centers. Science 269, 940-945
18. Katilius, E., Turanchik, T., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (1999) B-side electron transfer in a Rhodobacter sphaeroides reaction center mutant in which the B-side monomer bacteriochlorophyll is replaced with bacteriopheophytin. J. Phys. Chem. B 103, 7386-7389
19. Kirmaier, C., Gaul, D., DeBey, R., Holten, D., and Schenck, C. C. (1991) Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin. Science 251, 922-927 (Pubitemid 21926183)
20. Kirmaier, C., Laible, P. D., Czarnecki, K., Hata, A. N., Hanson, D. K., Bocian, D. F., and Holten, D. (2002) Comparison of M-side electron transfer in R. sphaeroides and R. capsulatus reaction centers. J. Phys. Chem. B 106, 1799-1808 (Pubitemid 35276070)
21. McDowell, L. M., Kirmaier, C., and Holten, D. (1990) Charge transfer and charge resonance states of the primary electron donor in wild-type and mutant bacterial reaction centers. Biochim. Biophys. Acta 1020, 239-246 (Pubitemid 120038262)
22. Watson, A. J., Fyfe, P. K., Frolov, D., Wakeham, M. C., Nabedryk, E., van Grondelle, R., Breton, J., and Jones, M. R. (2005) Replacement or exclusion of the B-branch bacteriopheophytin in the purple bacterial reaction centre: the H(B) cofactor is not required for assembly or core function of the Rhodobacter sphaeroides complex. Biochim. Biophys. Acta 1710, 34-46 (Pubitemid 41566997)
23. de Boer, A. L., Neerken, S., de Wijn, R., Permentier, H. P., Gast, P., Vijgenboom, E., and Hoff, A. J. (2002) High yield of B-branch electron transfer in a quadruple reaction center mutant of the photosynthetic bacterium Rhodobacter sphaeroides. Biochemistry 41, 3081-3088 (Pubitemid 34184639)
24. Laible, P. D., Kirmaier, C., Udawatte, C. S., Hofman, S. J., Holten, D., and Hanson, D. K. (2003) Quinone reduction via secondary B-branch electron transfer in mutant bacterial reaction centers. Biochemistry 42, 1718-1730 (Pubitemid 36205981)
25. A ubiquinone: possible insights into the evolution of reaction centres? Biochim. Biophys. Acta 1607, 53-63
26. Kirmaier, C., Holten, D., Bylina, E. J., and Youvan, D. C. (1988) Electron transfer in a genetically modified bacterial reaction center containing aheterodimer. Proc. Natl. Acad. Sci. U.S.A. 85, 7562-7566
27. Heller, B. A., Holten, D., and Kirmaier, C. (1995) Characterization of bacterial reaction centers having mutations of aromatic residues in the binding site of the bacteriopheophytin intermediary electron carrier. Biochemistry 34, 5294-5302
28. Robles, S. J., Breton, J., and Youvan, D. C. (1990) Partial symmetrization of the photosynthetic reaction center. Science 248, 1402-1405
29. Taguchi, A. K., Stocker, J. W., Alden, R. G., Causgrove, T. P., Peloquin, J. M., Boxer, S. G., and Woodbury, N. W. (1992) Biochemical characterization and electron-transfer reactions of sym1, a Rhodobacter capsulatus reaction center symmetry mutant which affects the initial electron donor. Biochemistry 31, 10345-10355
30. Haffa, A. L., Lin, S., Lobrutto, R., Williams, J. C., Taguchi, A. K., Allen, J. P., and Woodbury, N. W. (2005) Environmental control of primary photochemistry in a mutant bacterial reaction center. J. Phys. Chem. B 109, 19923-19928 (Pubitemid 41598506)
31. Kirmaier, C., He, C., and Holten, D. (2001) Manipulating the direction of electron transfer in the bacterial reaction center by swapping Phe for Tyr near BChl(M) (L181) and Tyr for Phe near BChl(L) (M208). Biochemistry 40, 12132-12139 (Pubitemid 32946554)
32. Kirmaier, C., Weems, D., and Holten, D. (1999) M-side electron transfer in reaction center mutants with a lysine near the nonphotoactive bacteriochlorophyll. Biochemistry 38, 11516-11530
33. Coleman, W. J., Bylina, E. J., Aumeier, W., Siegl, J., Eberl, U., Heckmann, R., Ogrodnik, A., Michel-Beyerle, M. E., and Youvan, D. C. (1990) in Structure and Function of Bacterial Photosynthetic Reaction Centers (Michel- Beyerle, M. E., ed) pp. 273-281, Springer-Verlag, New York
34. Coleman, W. J., and Youvan, D. C. (1993) Atavistic reaction centre. Nature 366, 517-518
35. Kirmaier, C., Laible, P. D., Hanson, D. K., and Holten, D. (2003) B-side charge separation in bacterial photosynthetic reaction centers: nanosecond time scale electron transfer from HB- to QB. Biochemistry 42, 2016-2024 (Pubitemid 36258675)
36. B site. Photosynth. Res. 64, 41-52
37. B) reduction by B-branch electron transfer in mutant bacterial reaction centers from Rhodobacter sphaeroides: quantum efficiency and x-ray structure. Biochemistry 44, 6920-6928
38. Chuang, J. I., Boxer, S. G., Holten, D., and Kirmaier, C. (2006) High yield of M-side electron transfer in mutants of Rhodobacter capsulatus reaction centers lacking the L-side bacteriopheophytin. Biochemistry 45, 3845-3851
39. Kee, H. L., Laible, P. D., Bautista, J. A., Hanson, D. K., Holten, D., and Kirmaier, C. (2006) Determination of the rate and yield of B-side quinone reduction in Rhodobacter capsulatus reaction centers. Biochemistry 45, 7314-7322 (Pubitemid 43877417)
40. Laible, P. D., Kirmaier, C. K., Holten, D., Tiede, D. M., Schiffer, M., and Hanson, D. K. (1998) in Photosynthesis: Mechanisms and Effects (Garab, G., ed) pp. 849-852, Kluwer, Dordrecht
41. A ubiquinone. FEBS Lett. 540, 234-240
42. Sambrook, J., Fritsch, E., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
43. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., 2nd, and Peterson, K. M. (1995) Four new derivatives of the broadhost- range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175-176
44. Bylina, E. J., Robles, S. J., and Youvan, D. C. (1988) Directed mutations affecting the putative bacteriochlorophyll-binding sites in the light-harvesting I antenna of Rhodobacter capsulatus. Isr. J. Chem. 28, 73-78
45. Weaver, P. F., Wall, J. D., and Gest, H. (1975) Characterization of Rhodopseudomonas capsulata. Arch. Microbiol. 105, 207-216
46. Kirmaier, C., Bautista, J. A., Laible, P. D., Hanson, D. K., and Holten, D. (2005) Probing the contribution of electronic coupling to the directionality of electron transfer in photosynthetic reaction centers. J. Phys. Chem. B 109, 24160-24172 (Pubitemid 43084729)
47. Bylina, E. J., Ismail, S., and Youvan, D. C. (1986) Plasmid pU29, a vehicle for mutagenesis of the photosynthetic puf operon in Rhodopseudomonas capsulata. Plasmid 16, 175-181 (Pubitemid 17230557)
48. Bylina, E. J., Jovine, R. V. M., and Youvan, D. C. (1989)Agenetic system for rapidly assessing herbicides that compete for the quinone binding site of photosynthetic reaction centers. Bio/Technology 7, 69-74
49. Youvan, D. C., Ismail, S., and Bylina, E. J. (1985) Gene 33, 19-30
50. Kirmaier, C., Laible, P. D., Hindin, E., Hanson, D. K., and Holten, D. (2003) Chem. Phys. 294, 305-318
51. Hanson, D. K., Baciou, L., Tiede, D. M., Nance, S. L., Schiffer, M., and Sebban, P. (1992) In bacterial reaction centers protons can diffuse to the secondary quinone by alternative pathways. Biochim. Biophys. Acta 1102, 260-265
52. Yuan, L., Kurek, I., English, J., and Keenan, R. (2005) Laboratory-directed protein evolution. Microbiol. Mol. Biol. Rev. 69, 373-392 (Pubitemid 41306743)
53. Jäckel, C., Kast, P., and Hilvert, D. (2008) Protein design by directed evolution. Annu. Rev. Biophys. 37, 153-173
54. Bokma, E., Koronakis, E., Lobedanz, S., Hughes, C., and Koronakis, V. (2006) Directed evolution of a bacterial efflux pump: adaptation of the E. coli TolC exit duct to the Pseudomonas MexAB translocase. FEBS Lett. 580, 5339-5343 (Pubitemid 44415819)
55. Dong, S., Rogan, S. C., and Roth, B. L. (2010) Directed molecular evolution of DREADDs: A generic approach to creating next-generation RASSLs. Nat. Protocols 5, 561-573
56. Sarkar, C. A., Dodevski, I., Kenig, M., Dudli, S., Mohr, A., Hermans, E., and Plückthun, A. (2008) Directed evolution of a G protein-coupled receptor for expression, stability, and binding selectivity. Proc. Natl. Acad. Sci. U.S.A. 105, 14808-14813
57. Wise, K. J., Gillespie, N. B., Stuart, J. A., Krebs, M. P., and Birge, R. R. (2002) Optimization of bacteriorhodopsin for bioelectronic devices. Trends Biotechnol. 20, 387-394 (Pubitemid 34880174)
58. Jia, Y., DiMagno, T. J., Chan, C. K., Wang, Z., Du, M., Hanson, D. K., Schiffer, M., Norris, J. R., Fleming, G. R., and Popov, M. S. (1993) Primary charge separation in mutant reaction centers of Rhodobacter capsulatus. J. Phys. Chem. 97, 13180-13191