Literature DB >> 28743751

Nature does not rely on long-lived electronic quantum coherence for photosynthetic energy transfer.

Hong-Guang Duan1,2,3, Valentyn I Prokhorenko1, Richard J Cogdell4, Khuram Ashraf4, Amy L Stevens1,3,5,6, Michael Thorwart7,3, R J Dwayne Miller8,3,5,6.   

Abstract

During the first steps of photosynthesis, the energy of impinging solar photons is transformed into electronic excitation energy of the light-harvesting biomolecular complexes. The subsequent energy transfer to the reaction center is commonly rationalized in terms of excitons moving on a grid of biomolecular chromophores on typical timescales [Formula: see text]100 fs. Today's understanding of the energy transfer includes the fact that the excitons are delocalized over a few neighboring sites, but the role of quantum coherence is considered as irrelevant for the transfer dynamics because it typically decays within a few tens of femtoseconds. This orthodox picture of incoherent energy transfer between clusters of a few pigments sharing delocalized excitons has been challenged by ultrafast optical spectroscopy experiments with the Fenna-Matthews-Olson protein, in which interference oscillatory signals up to 1.5 ps were reported and interpreted as direct evidence of exceptionally long-lived electronic quantum coherence. Here, we show that the optical 2D photon echo spectra of this complex at ambient temperature in aqueous solution do not provide evidence of any long-lived electronic quantum coherence, but confirm the orthodox view of rapidly decaying electronic quantum coherence on a timescale of 60 fs. Our results can be considered as generic and give no hint that electronic quantum coherence plays any biofunctional role in real photoactive biomolecular complexes. Because in this structurally well-defined protein the distances between bacteriochlorophylls are comparable to those of other light-harvesting complexes, we anticipate that this finding is general and directly applies to even larger photoactive biomolecular complexes.

Keywords:  2D spectroscopy; Fenna–Matthews–Olson protein; exciton; photosynthesis; quantum coherence

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Year:  2017        PMID: 28743751      PMCID: PMC5559008          DOI: 10.1073/pnas.1702261114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

Review 1.  Lessons from nature about solar light harvesting.

Authors:  Gregory D Scholes; Graham R Fleming; Alexandra Olaya-Castro; Rienk van Grondelle
Journal:  Nat Chem       Date:  2011-09-23       Impact factor: 24.427

2.  The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria.

Authors:  Dale E Tronrud; Jianzhong Wen; Leslie Gay; Robert E Blankenship
Journal:  Photosynth Res       Date:  2009-05-13       Impact factor: 3.573

3.  Comment on "Coherence and uncertainty in nanostructured organic photovoltaics".

Authors:  Shaul Mukamel
Journal:  J Phys Chem A       Date:  2013-09-26       Impact factor: 2.781

4.  Demonstration and interpretation of significant asymmetry in the low-resolution and high-resolution Q(y) fluorescence and absorption spectra of bacteriochlorophyll a.

Authors:  Margus Rätsep; Zheng-Li Cai; Jeffrey R Reimers; Arvi Freiberg
Journal:  J Chem Phys       Date:  2011-01-14       Impact factor: 3.488

5.  Equivalence of quantum and classical coherence in electronic energy transfer.

Authors:  John S Briggs; Alexander Eisfeld
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2011-05-12

6.  Two-dimensional spectroscopy of a molecular dimer unveils the effects of vibronic coupling on exciton coherences.

Authors:  Alexei Halpin; Philip J M Johnson; Roel Tempelaar; R Scott Murphy; Jasper Knoester; Thomas L C Jansen; R J Dwayne Miller
Journal:  Nat Chem       Date:  2014-01-12       Impact factor: 24.427

7.  Structure of a bacteriochlorophyll-protein from the green photosynthetic bacterium Chlorobium limicola: crystallographic evidence for a trimer.

Authors:  R E Fenna; B W Matthews; J M Olson; E K Shaw
Journal:  J Mol Biol       Date:  1974-04-05       Impact factor: 5.469

8.  Theory and Simulation of the Environmental Effects on FMO Electronic Transitions.

Authors:  Carsten Olbrich; Johan Strümpfer; Klaus Schulten; Ulrich Kleinekathöfer
Journal:  J Phys Chem Lett       Date:  2011-06-30       Impact factor: 6.475

9.  Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting.

Authors:  Jianzhong Wen; Hao Zhang; Michael L Gross; Robert E Blankenship
Journal:  Proc Natl Acad Sci U S A       Date:  2009-04-01       Impact factor: 11.205

10.  Origin of long-lived coherences in light-harvesting complexes.

Authors:  Niklas Christensson; Harald F Kauffmann; Tõnu Pullerits; Tomáš Mančal
Journal:  J Phys Chem B       Date:  2012-06-14       Impact factor: 2.991

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  38 in total

1.  Neutron and X-ray analysis of the Fenna-Matthews-Olson photosynthetic antenna complex from Prosthecochloris aestuarii.

Authors:  Xun Lu; Brinda Selvaraj; Sudipa Ghimire-Rijal; Gregory S Orf; Flora Meilleur; Robert E Blankenship; Matthew J Cuneo; Dean A A Myles
Journal:  Acta Crystallogr F Struct Biol Commun       Date:  2019-02-20       Impact factor: 1.056

2.  VenusA206 Dimers Behave Coherently at Room Temperature.

Authors:  Youngchan Kim; Henry L Puhl; Eefei Chen; Grace H Taumoefolau; Tuan A Nguyen; David S Kliger; Paul S Blank; Steven S Vogel
Journal:  Biophys J       Date:  2019-04-22       Impact factor: 4.033

Review 3.  The future of quantum biology.

Authors:  Adriana Marais; Betony Adams; Andrew K Ringsmuth; Marco Ferretti; J Michael Gruber; Ruud Hendrikx; Maria Schuld; Samuel L Smith; Ilya Sinayskiy; Tjaart P J Krüger; Francesco Petruccione; Rienk van Grondelle
Journal:  J R Soc Interface       Date:  2018-11-14       Impact factor: 4.118

Review 4.  Coherent phenomena in photosynthetic light harvesting: part two-observations in biological systems.

Authors:  Harry W Rathbone; Jeffery A Davis; Katharine A Michie; Sophia C Goodchild; Neil O Robertson; Paul M G Curmi
Journal:  Biophys Rev       Date:  2018-09-22

5.  Temperature-dependent conformations of exciton-coupled Cy3 dimers in double-stranded DNA.

Authors:  Loni Kringle; Nicolas P D Sawaya; Julia Widom; Carson Adams; Michael G Raymer; Alán Aspuru-Guzik; Andrew H Marcus
Journal:  J Chem Phys       Date:  2018-02-28       Impact factor: 3.488

6.  Dynamics of diverse coherences in primary charge separation of bacterial reaction center at 77 K revealed by wavelet analysis.

Authors:  Fei Ma; Elisabet Romero; Michael R Jones; Vladimir I Novoderezhkin; Long-Jiang Yu; Rienk van Grondelle
Journal:  Photosynth Res       Date:  2021-10-28       Impact factor: 3.573

Review 7.  Recent progress in atomistic modeling of light-harvesting complexes: a mini review.

Authors:  Sayan Maity; Ulrich Kleinekathöfer
Journal:  Photosynth Res       Date:  2022-10-07       Impact factor: 3.429

8.  Excitation energy transfer and vibronic coherence in intact phycobilisomes.

Authors:  Sourav Sil; Ryan W Tilluck; Nila Mohan T M; Chase H Leslie; Justin B Rose; Maria Agustina Domínguez-Martín; Wenjing Lou; Cheryl A Kerfeld; Warren F Beck
Journal:  Nat Chem       Date:  2022-09-19       Impact factor: 24.274

9.  Electronic Conductance Resonance in Non-Redox-Active Proteins.

Authors:  Bintian Zhang; Weisi Song; Jesse Brown; Robert Nemanich; Stuart Lindsay
Journal:  J Am Chem Soc       Date:  2020-03-23       Impact factor: 15.419

Review 10.  2D Electronic Spectroscopic Techniques for Quantum Technology Applications.

Authors:  Elisabetta Collini
Journal:  J Phys Chem C Nanomater Interfaces       Date:  2021-06-11       Impact factor: 4.126

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