Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy

Energy transfer and trapping in the light harvesting antennae of purple photosynthetic bacteria is an ultrafast process, which occurs with a quantum efficiency close to unity. However the mechanisms behind this process have not yet been fully understood. Recently it was proposed that low-lying energy dark states, such as charge transfer states and polaron pairs, play an important role in the dynamics and directionality of energy transfer. However, it is difficult to directly detect those states because of their small transition dipole moment and overlap with the B850/B870 exciton bands. Here we present a new experimental approach, which combines the selectivity of two-dimensional electronic spectroscopy with the availability of genetically modified light harvesting complexes, to reveal the presence of those dark states in both the genetically modified and the wild-type light harvesting 2 complexes of Rhodopseudomonas palustris. We suggest that Nature has used the unavoidable charge transfer processes that occur when LH pigments are concentrated to enhance and direct the flow of energy.

[1]  Graham R Fleming,et al.  Coherence quantum beats in two-dimensional electronic spectroscopy. , 2008, The journal of physical chemistry. A.

[2]  Vladimir I. Novoderezhkin,et al.  Quantum Coherence in Photosynthesis for Efficient Solar Energy Conversion , 2014, Nature Physics.

[3]  Javier Prior,et al.  The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment–protein complexes , 2013, Nature Physics.

[4]  G. Scholes,et al.  Broadband 2D Electronic Spectroscopy Reveals a Carotenoid Dark State in Purple Bacteria , 2013, Science.

[5]  R. van Grondelle,et al.  Mixing of exciton and charge-transfer states in Photosystem II reaction centers: modeling of Stark spectra with modified Redfield theory. , 2007, Biophysical journal.

[6]  Graham R Fleming,et al.  Phase-stabilized two-dimensional electronic spectroscopy. , 2004, The Journal of chemical physics.

[7]  D. Abramavičius,et al.  Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment–protein complexes , 2015, Photosynthesis Research.

[8]  Ryan D. Pensack,et al.  Charge Photogeneration in Neat Conjugated Polymers , 2014 .

[9]  R. van Grondelle,et al.  The nature of coherences in the B820 bacteriochlorophyll dimer revealed by two-dimensional electronic spectroscopy. , 2014, Physical chemistry chemical physics : PCCP.

[10]  Peter D Dahlberg,et al.  Timescales of Coherent Dynamics in the Light Harvesting Complex 2 (LH2) of Rhodobacter sphaeroides. , 2013, The journal of physical chemistry letters.

[11]  G. Scholes.  Insights into excitons confined to nanoscale systems: electron-hole interaction, binding energy, and photodissociation. , 2008, ACS nano.

[12]  Graham R Fleming,et al.  Lessons from nature about solar light harvesting. , 2011, Nature chemistry.

[13]  R. Monshouwer,et al.  Disordered exciton model for the core light-harvesting antenna of Rhodopseudomonas viridis. , 1999, Biophysical journal.

[14]  Tõnu Pullerits,et al.  Photosynthetic light-harvesting: Reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit , 1999 .

[15]  Graham R Fleming,et al.  Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex , 2006, Proceedings of the National Academy of Sciences.

[16]  N. Isaacs,et al.  The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. , 2001, Biochemistry.

[17]  Gregory D Scholes,et al.  The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. , 2012, The Journal of chemical physics.

[18]  V. Sundström,et al.  Exciton Relaxation and Polaron Formation in LH2 at Low Temperature , 2000 .

[19]  Tõnu Pullerits,et al.  Origin of Long-Lived Coherences in Light-Harvesting Complexes , 2012, The journal of physical chemistry. B.

[20]  Rienk van Grondelle,et al.  Energy transfer in photosynthesis: experimental insights and quantitative models. , 2006, Physical chemistry chemical physics : PCCP.

[21]  I. V. van Stokkum,et al.  Two different charge separation pathways in photosystem II. , 2010, Biochemistry.

[22]  Jennifer P Ogilvie,et al.  Probing Photosynthetic Energy and Charge Transfer with Two-Dimensional Electronic Spectroscopy. , 2012, The journal of physical chemistry letters.

[23]  S. Mukamel,et al.  Excitonic interactions and Stark spectroscopy of light-harvesting systems. , 1998 .

[24]  G. Scholes,et al.  Coherent Energy Transfer under Incoherent Light Conditions. , 2012, The journal of physical chemistry letters.

[25]  S. Boxer,et al.  Characterization of the Light-Harvesting Antennas of Photosynthetic Purple Bacteria by Stark Spectroscopy. 1. LH1 Antenna Complex and the B820 Subunit from Rhodospirillum rubrum , 1997 .

[26]  T. Mančal,et al.  Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems , 2007, Nature.

[27]  R. Monshouwer,et al.  Exciton (De)Localization in the LH2 Antenna of Rhodobacter sphaeroides As Revealed by Relative Difference Absorption Measurements of the LH2 Antenna and the B820 Subunit , 1999 .

[28]  G. Fleming,et al.  Electronic Excitation Transfer in the LH2 Complex of Rhodobacter sphaeroides , 1996 .

[29]  J. Sturgis,et al.  Ultrafast excited state processes in Roseobacter denitrificans antennae: comparison of isolated complexes and native membranes. , 2014, Physical chemistry chemical physics : PCCP.

[30]  V. Sundström,et al.  Energy transfer and trapping in photosynthesis , 1994 .

[31]  G. Fleming,et al.  Primary steps of photosynthesis , 1994 .

[32]  William K. Peters,et al.  Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework , 2012, Proceedings of the National Academy of Sciences.

[33]  R. Grondelle.  Excitation energy transfer, trapping and annihilation in photosynthetic systems , 1985 .

[34]  Andrew F Fidler,et al.  Real-time mapping of electronic structure with single-shot two-dimensional electronic spectroscopy , 2010, Proceedings of the National Academy of Sciences.

[35]  R. van Grondelle,et al.  Dynamics of exciton relaxation in LH2 antenna probed by multipulse nonlinear spectroscopy. , 2011, The journal of physical chemistry. A.

[36]  G. Lanzani,et al.  Low light adaptation: energy transfer processes in different types of light harvesting complexes from Rhodopseudomonas palustris. , 2009, Biophysical journal.

[37]  D. Abramavičius,et al.  Static and Dynamic Disorder in Bacterial Light-Harvesting Complex LH2: A 2DES Simulation Study. , 2014, The journal of physical chemistry. B.

[38]  R. Cogdell,et al.  Single-molecule spectroscopy reveals that individual low-light LH2 complexes from Rhodopseudomonas palustris 2.1.6. have a heterogeneous polypeptide composition. , 2009, Biophysical journal.

[39]  R. Grondelle,et al.  Intra- and interband transfers in the B800-B850 antenna of Rhodospirillum molischianum Redfield theory modeling of polarized pump-probe kinetics , 2003 .

[40]  V. Sundström,et al.  B800-->B850 energy transfer mechanism in bacterial LH2 complexes investigated by B800 pigment exchange. , 2000, Biophysical journal.

[41]  G. Porter,et al.  Concentration quenching in chlorophyll , 1976, Nature.

[42]  R. van Grondelle,et al.  How exciton-vibrational coherences control charge separation in the photosystem II reaction center. , 2015, Physical chemistry chemical physics : PCCP.