Mutations to R. sphaeroides Reaction Center Perturb Energy Levels and Vibronic Coupling but Not Observed Energy Transfer Rates

Journal of Physical Chemistry A

Volumn 120, Issue 9, 2016, Pages 1479-1487

  Flanagan, Moira L ^a   Long, Phillip D ^a   Dahlberg, Peter D ^a   Rolczynski, Brian S ^a   Massey, Sara C ^a   Engel, Gregory S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; CHROMOPHORES; COLLECTOR EFFICIENCY; ELECTRIC EXCITATION; ENERGY TRANSFER; EXCITED STATES;

BACTERIAL REACTION; BACTERIOCHLOROPHYLLS; ELECTRONIC COHERENCE; ELECTRONIC EXCITED STATE; ENERGY TRANSFER DYNAMICS; ENERGY-TRANSFER RATE; RHODOBACTER SPHAEROIDES; VIBRATIONAL MOTIONS;

REACTION RATES;

PHOTOSYNTHESIS;

ENERGY TRANSFER; GENETICS; MUTATION; PHOTOSYNTHESIS; PROCEDURES; RHODOBACTER SPHAEROIDES; SPECTROSCOPY;

ENERGY TRANSFER; MUTATION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES; SPECTRUM ANALYSIS;

EID: 84960424709     PISSN: 10895639     EISSN: 15205215     Source Type: Journal    
DOI: 10.1021/acs.jpca.5b08366     Document Type: Article

References (59)

1. van Amerongen, H.; Valkunas, L.; van Grondelle, R. Photosynthetic Excitons; World Scientific: River Edge, NJ, 2000.
2. Arnett, D. C.; Moser, C. C.; Dutton, P. L.; Scherer, N. F. The First Events in Photosynthesis: Electronic Coupling and Energy Transfer Dynamics in the Photosynthetic Reaction Center from Rhodobacter Sphaeroides J. Phys. Chem. B 1999, 103, 2014-2032 10.1021/jp984464j
3. Jordanides, X. J.; Scholes, G. D.; Fleming, G. R. The Mechanism of Energy Transfer in the Bacterial Photosynthetic Reaction Center J. Phys. Chem. B 2001, 105, 1652-1669 10.1021/jp003572e
4. Parkinson, D. Y.; Lee, H.; Fleming, G. R. Measuring Electronic Coupling in the Reaction Center of Purple Photosynthetic Bacteria by Two-Color, Three-Pulse Photon Echo Peak Shift Spectroscopy J. Phys. Chem. B 2007, 111, 7449-7456 10.1021/jp070029q
5. Scholes, G. D.; Fleming, G. R.; Olaya-Castro, A.; van Grondelle, R. Lessons from Nature About Solar Light Harvesting Nat. Chem. 2011, 3, 763-774 10.1038/nchem.1145
6. Lee, H.; Cheng, Y.-C.; Fleming, G. R. Coherence Dynamics in Photosynthesis: Protein Protection of Excitonic Coherence Science 2007, 316, 1462-1465 10.1126/science.1142188
7. Turner, D. B.; Dinshaw, R.; Lee, K.-K.; Belsley, M. S.; Wilk, K. E.; Curmi, P. M. G.; Scholes, G. D. Quantitative Investigations of Quantum Coherence for a Light-Harvesting Protein at Conditions Simulating Photosynthesis Phys. Chem. Chem. Phys. 2012, 14, 4857-4874 10.1039/c2cp23670b
8. Christensson, N.; Kauffmann, H. F.; Pullerits, T.; Mancal, T. Origin of Long-Lived Coherences in Light-Harvesting Complexes J. Phys. Chem. B 2012, 116, 7449-7454 10.1021/jp304649c
9. Blankenship, R. E. Molecular Mechanisms of Photosynthesis; Blackwell Science: Oxford, Malden, MA, 2002.
10. Cherepy, N. J.; Shreve, A. P.; Moore, L. J.; Boxer, S. G.; Mathies, R. A. Electronic and Nuclear Dynamics of the Accessory Bacteriochlorophylls in Bacterial Photosynthetic Reaction Centers from Resonance Raman Intensities J. Phys. Chem. B 1997, 101, 3250-3260 10.1021/jp963051k
11. Brixner, T.; Mancal, T.; Stiopkin, I. V.; Fleming, G. R. Phase-Stabilized Two-Dimensional Electronic Spectroscopy J. Chem. Phys. 2004, 121, 4221-4236 10.1063/1.1776112
12. Cowan, M. L.; Ogilvie, J. P.; Miller, R. J. D. Two-Dimensional Spectroscopy Using Diffractive Optics Based Phased-Locked Photon Echoes Chem. Phys. Lett. 2004, 386, 184-189 10.1016/j.cplett.2004.01.027
13. Hybl, J. D.; Albrecht, A. W.; Faeder, S. M. G.; Jonas, D. M. Two-Dimensional Electronic Spectroscopy Chem. Phys. Lett. 1998, 297, 307-313 10.1016/S0009-2614(98)01140-3
14. Arnett, D. C.; Yang, T.-S.; Scherer, N. F. Optical and Vibrational Coherence in Bacteriochlorophyll A. In Time-Resolved Vib. Spectrosc., Proc. Int. Conf. TRVS; Los Alamos National Labs: Santa Fe, NM, 1997; pp 131-135.
15. Chenu, A.; Christensson, N.; Kauffmann, H. F.; Mancal, T. Enhancement of Vibronic and Ground-State Vibrational Coherences in 2D Spectra of Photosynthetic Complexes Sci. Rep. 2013, 3, 2029 10.1038/srep02029
16. Engel, G. S.; Calhoun, T. R.; Read, E. L.; Ahn, T.-K.; Mancal, T.; Cheng, Y.-C.; Blankenship, R. E.; Fleming, G. R. Evidence for Wavelike Energy Transfer through Quantum Coherence in Photosynthetic Systems Nature 2007, 446, 782-786 10.1038/nature05678
17. Kreisbeck, C.; Kramer, T. Long-Lived Electronic Coherence in Dissipative Exciton Dynamics of Light-Harvesting Complexes J. Phys. Chem. Lett. 2012, 3, 2828-2833 10.1021/jz3012029
18. Lim, J.; Palecek, D.; Caycedo-Soler, F.; Lincoln, C. N.; Prior, J.; von Berlepsch, H.; Huelga, S. F.; Plenio, M. B.; Zigmantas, D.; Hauer, J. Vibronic Origin of Long-Lived Coherence in an Artificial Molecular Light Harvester Nat. Commun. 2015, 6, 7755 10.1038/ncomms8755
19. Milota, F.; Prokhorenko, V. I.; Mancal, T.; von Berlepsch, H.; Bixner, O.; Kauffmann, H. F.; Hauer, J. Vibronic and Vibrational Coherences in Two-Dimensional Electronic Spectra of Supramolecular J-Aggregates J. Phys. Chem. A 2013, 117, 6007-6014 10.1021/jp3119605
20. Plenio, M. B.; Almeida, J.; Huelga, S. F. Origin of Long-Lived Oscillations in 2D-Spectra of a Quantum Vibronic Model: Electronic Versus Vibrational Coherence J. Chem. Phys. 2013, 139, 235102 10.1063/1.4846275
21. Romero, E.; Augulis, R.; Novoderezhkin, V. I.; Ferretti, M.; Thieme, J.; Zigmantas, D.; van Grondelle, R. Quantum Coherence in Photosynthesis for Efficient Solar-Energy Conversion Nat. Phys. 2014, 10, 676-683 10.1038/nphys3017
22. Ryu, I. S.; Dong, H.; Fleming, G. R. Role of Electronic-Vibrational Mixing in Enhancing Vibrational Coherences in the Ground Electronic States of Photosynthetic Bacterial Reaction Center J. Phys. Chem. B 2014, 118, 1381-1388 10.1021/jp4100476
23. Turner, D. B.; Wilk, K. E.; Curmi, P. M. G.; Scholes, G. D. Comparison of Electronic and Vibrational Coherence Measured by Two-Dimensional Electronic Spectroscopy J. Phys. Chem. Lett. 2011, 2, 1904-1911 10.1021/jz200811p
24. Butkus, V.; Zigmantas, D.; Valkunas, L.; Abramavicius, D. Vibrational Vs. Electronic Coherences in 2D Spectrum of Molecular Systems Chem. Phys. Lett. 2012, 545, 40-43 10.1016/j.cplett.2012.07.014
25. Chin, A. W.; Prior, J.; Rosenbach, R.; Caycedo-Soler, F.; Huelga, S. F.; Plenio, M. B. The Role of Non-Equilibrium Vibrational Structures in Electronic Coherence and Recoherence in Pigment-Protein Complexes Nat. Phys. 2013, 9, 113-118 10.1038/nphys2515
26. Butkus, V.; Valkunas, L.; Abramavicius, D. Vibronic Phenomena and Exciton-Vibrational Interference in Two-Dimensional Spectra of Molecular Aggregates J. Chem. Phys. 2014, 140, 034306 10.1063/1.4861466
27. Fuller, F. D.; Pan, J.; Gelzinis, A.; Butkus, V.; Senlik, S. S.; Wilcox, D. E.; Yocum, C. F.; Valkunas, L.; Abramavicius, D.; Ogilvie, J. P. Vibronic Coherence in Oxygenic Photosynthesis Nat. Chem. 2014, 6, 706-711 10.1038/nchem.2005
28. Panitchayangkoon, G.; Hayes, D.; Fransted, K. A.; Caram, J. R.; Harel, E.; Wen, J. Z.; Blankenship, R. E.; Engel, G. S. Long-Lived Quantum Coherence in Photosynthetic Complexes at Physiological Temperature Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 12766-12770 10.1073/pnas.1005484107
29. Hayes, D.; Wen, J.; Panitchayangkoon, G.; Blankenship, R. E.; Engel, G. S. Robustness of Electronic Coherence in the Fenna-Matthews-Olson Complex to Vibronic and Structural Modifications Faraday Discuss. 2011, 150, 459-469 10.1039/c0fd00030b
30. Goldsmith, J. O.; Boxer, S. G. Rapid Isolation of Bacterial Photosynthetic Reaction Centers with an Engineered Poly-Histidine Tag Biochim. Biophys. Acta, Bioenerg. 1996, 1276, 171-175 10.1016/0005-2728(96)00091-6
31. Zheng, H. B.; Caram, J. R.; Dahlberg, P. D.; Rolczynski, B. S.; Viswanathan, S.; Dolzhnikov, D. S.; Khadivi, A.; Talapin, D. V.; Engel, G. S. Dispersion-Free Continuum Two-Dimensional Electronic Spectrometer Appl. Opt. 2014, 53, 1909-1917 10.1364/AO.53.001909
32. Caram, J. R.; Zheng, H. B.; Dahlberg, P. D.; Rolczynski, B. S.; Griffin, G. B.; Dolzhnikov, D. S.; Talapin, D. V.; Engel, G. S. Exploring Size and State Dynamics in Cdse Quantum Dots Using Two-Dimensional Electronic Spectroscopy J. Chem. Phys. 2014, 140, 084701 10.1063/1.4865832
33. Singh, V. P.; Fidler, A. F.; Rolczynski, B. S.; Engel, G. S. Independent Phasing of Rephasing and Non-Rephasing 2D Electronic Spectra J. Chem. Phys. 2013, 139, 084201 10.1063/1.4818808
34. Williams, J. C.; Haffa, A. L. M.; McCulley, J. L.; Woodbury, N. W.; Allen, J. P. Electrostatic Interactions between Charged Amino Acid Residues and the Bacteriochlorophyll Dimer in Reaction Centers from Rhodobacter Sphaeroides Biochemistry 2001, 40, 15403-15407 10.1021/bi011574z
35. Cho, M. H.; Brixner, T.; Stiopkin, I.; Vaswani, H.; Fleming, G. R. Two Dimensional Electronic Spectroscopy of Molecular Complexes J. Chin. Chem. Soc. 2006, 53, 15-24 10.1002/jccs.200600002
36. Westenhoff, S.; Palec ek, D.; Edlund, P.; Smith, P.; Zigmantas, D. Coherent Picosecond Exciton Dynamics in a Photosynthetic Reaction Center J. Am. Chem. Soc. 2012, 134, 16484-16487 10.1021/ja3065478
37. Jia, Y.; Jonas, D. M.; Joo, T.; Nagasawa, Y.; Lang, M. J.; Fleming, G. R. Observation of Ultrafast Energy Transfer from the Accessory Bacteriochlorophylls to the Special Pair in Photosynthetic Reaction Centers J. Phys. Chem. 1995, 99, 6263-6266 10.1021/j100017a001
38. Vos, M. H.; Breton, J.; Martin, J.-L. Electronic Energy Transfer within the Hexamer Cofactor System of Bacterial Reaction Centers J. Phys. Chem. B 1997, 101, 9820-9832 10.1021/jp971486h
39. Myers, J. A.; Lewis, K. L. M.; Fuller, F. D.; Tekavec, P. F.; Yocum, C. F.; Ogilvie, J. P. Two-Dimensional Electronic Spectroscopy of the D1-D2-Cyt B559 Photosystem Ii Reaction Center Complex J. Phys. Chem. Lett. 2010, 1, 2774-2780 10.1021/jz100972z
40. Kramer, T.; Kreisbeck, C. In Modelling Excitonic-Energy Transfer in Light-Harvesting Complexes; AIP Conference Proceedings; AIP: Melville, NY, 2014.
41. Cherepy, N. J.; Shreve, A. P.; Moore, L. J.; Boxer, S. G.; Mathies, R. A. Temperature Dependence of the Qy Resonance Raman Spectra of Bacteriochlorophylls, the Primary Electron Donor, and Bacteriopheophytins in the Bacterial Photosynthetic Reaction Center Biochemistry 1997, 36, 8559-8566 10.1021/bi970024r
42. Cherepy, N. J.; Shreve, A. P.; Moore, L. J.; Franzen, S.; Boxer, S. G.; Mathies, R. A. Near-Infrared Resonance Raman-Spectroscopy of the Special Pair and the Accessory Bacteriochlorophylls in Photosynthetic Reaction Centers J. Phys. Chem. 1994, 98, 6023-6029 10.1021/j100074a032
43. Shreve, A. P.; Cherepy, N. J.; Franzen, S.; Boxer, S. G.; Mathies, R. A. Rapid-Flow Resonance Raman-Spectroscopy of Bacterial Photosynthetic Reaction Centers Proc. Natl. Acad. Sci. U. S. A. 1991, 88, 11207-11211 10.1073/pnas.88.24.11207
44. del Rey, M.; Chin, A. W.; Huelga, S. F.; Plenio, M. B. Exploiting Structured Environments for Efficient Energy Transfer: The Phonon Antenna Mechanism J. Phys. Chem. Lett. 2013, 4, 903-907 10.1021/jz400058a
45. Sato, Y.; Doolittle, B. Influence of Intra-Pigment Vibrations on Dynamics of Photosynthetic Exciton J. Chem. Phys. 2014, 141, 185102 10.1063/1.4901056
46. Perlik, V.; Seibt, J.; Cranston, L. J.; Cogdell, R. J.; Lincoln, C. N.; Savolainen, J.; Sanda, F.; Mancal, T.; Hauer, J. Vibronic Coupling Explains the Ultrafast Carotenoid-to-Bacteriochlorophyll Energy Transfer in Natural and Artificial Light Harvesters J. Chem. Phys. 2015, 142, 212434 10.1063/1.4919548
47. Womick, J. M.; West, B.; Scherer, N. F.; Moran, A. M. Vibronic Effects in the Spectroscopy and Dynamics of C-Phycocyanin J. Phys. B: At., Mol. Opt. Phys. 2012, 45, 154016 10.1088/0953-4075/45/15/154016
48. Womick, J. M.; Moran, A. M. Vibronic Enhancement of Exciton Sizes and Energy Transport in Photosynthetic Complexes J. Phys. Chem. B 2011, 115, 1347-1356 10.1021/jp106713q
49. Tiwari, V.; Peters, W. K.; Jonas, D. M. Electronic Resonance with Anticorrelated Pigment Vibrations Drives Photosynthetic Energy Transfer Outside the Adiabatic Framework Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 1203-1208 10.1073/pnas.1211157110
50. Seibt, J.; Pullerits, T. Beating Signals in 2D Spectroscopy: Electronic or Nuclear Coherences? Application to a Quantum Dot Model System J. Phys. Chem. C 2013, 117, 18728-18737 10.1021/jp406103m
51. Dostal, J.; Mancal, T.; Vacha, F.; Psencik, J.; Zigmantas, D. Unraveling the Nature of Coherent Beatings in Chlorosomes J. Chem. Phys. 2014, 140, 115103 10.1063/1.4868557
52. Panitchayangkoon, G.; Voronine, D. V.; Abramavicius, D.; Caram, J. R.; Lewis, N. H. C.; Mukamel, S.; Engel, G. S. Direct Evidence of Quantum Transport in Photosynthetic Light-Harvesting Complexes Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 20908-20912 10.1073/pnas.1105234108
53. Tekavec, P. E.; Myers, J. A.; Lewis, K. L. M.; Ogilvie, J. P. Two-Dimensional Electronic Spectroscopy with a Continuum Probe Opt. Lett. 2009, 34, 1390-1392 10.1364/OL.34.001390
54. Caram, J. R.; Fidler, A. F.; Engel, G. S. Excited and Ground State Vibrational Dynamics Revealed by Two-Dimensional Electronic Spectroscopy J. Chem. Phys. 2012, 137, 024507 10.1063/1.4733710
55. Senlik, S. S.; Policht, V. R.; Ogilvie, J. P. Two-Color Nonlinear Spectroscopy for the Rapid Acquisition of Coherent Dynamics J. Phys. Chem. Lett. 2015, 6, 2413-20 10.1021/acs.jpclett.5b00861
56. Egorova, D.; Gelin, M. F.; Domcke, W. Analysis of Cross Peaks in Two-Dimensional Electronic Photon-Echo Spectroscopy for Simple Models with Vibrations and Dissipation J. Chem. Phys. 2007, 126, 074314 10.1063/1.2435353
57. Faeder, S. M. G.; Jonas, D. M. Two-Dimensional Electronic Correlation and Relaxation Spectra: Theory and Model Calculations J. Phys. Chem. A 1999, 103, 10489-10505 10.1021/jp9925738
58. Bardeen, C. J.; Wang, Q.; Shank, C. V. Selective Excitation of Vibrational Wave-Packet Motion Using Chirped Pulses Phys. Rev. Lett. 1995, 75, 3410-3413 10.1103/PhysRevLett.75.3410
59. Fransted, K. A.; Caram, J. R.; Hayes, D.; Engel, G. S. Two-Dimensional Electronic Spectroscopy of Bacteriochlorophyll a in Solution: Elucidating the Coherence Dynamics of the Fenna-Matthews-Olson Complex Using Its Chromophore as a Control J. Chem. Phys. 2012, 137, 125101 10.1063/1.4752107