Fenna–Matthews–Olson complex

The Fenna–Matthews–Olson (FMO) complex is a water-soluble complex and was the first pigment-protein complex (PPC) to be structure analyzed by x-ray spectroscopy.[2] It appears in green sulfur bacteria and mediates the excitation energy transfer from light-harvesting chlorosomes to the membrane-embedded bacterial reaction center (bRC). Its structure is trimeric (C3-symmetry). Each of the three monomers contains eight bacteriochlorophyll a (BChl a) molecules. They are bound to the protein scaffold via chelation of their central magnesium atom either to amino acids of the protein (mostly histidine) or water-bridged oxygen atoms (only one BChl a of each monomer).

Figure 1. The FMO protein trimer.[1] The BChl a molecules are depicted in green, the central magnesium atom in red and the protein in grey ("cartoons" representation). Each monomer contains bacteriochlorophylls.

Since the structure is available, calculating structure-based optical spectra is possible for comparison with experimental optical spectra.[3][4] In the simplest case only the excitonic coupling of the BChls is taken into account.[5] More realistic theories consider pigment-protein coupling.[6] An important property is the local transition energy (site energy) of the BChls, different for each, due to their individual local protein environment. The site energies of the BChls determine the direction of the energy flow.

Some structural information on the FMO-RC super complex is available, which was obtained by electron microscopy[7][8] and linear dichroism spectra measured on FMO trimers and FMO-RC complexes. From these measurements, two orientations of the FMO complex relative to the RC are possible. The orientation with BChl 3 and 4 close to the RC and BChl 1 and 6 (following Fenna and Matthews' original numbering) oriented towards the chlorosomes is useful for efficient energy transfer.[9]

Test object

The complex is the simplest PPC appearing in nature and therefore a suitable test object for the development of methods that can be transferred to more complex systems like photosystem I. Engel and co-workers observed that the FMO complex exhibits remarkably long quantum coherence,[10] but after about a decade of debate, it was shown that this quantum coherence has no significance to the functioning of the complex.[11] Furthermore, it was shown that the reported long lived oscillations observed in the spectra are solely due to groundstate vibrational dynamics and do not reflect any energy transfer dynamics.[12]

Quantum light harvesting

Light harvesting in photosynthesis employs both classical and quantum mechanical processes with an energy efficiency of almost 100 percent. For light to produce energy in classical processes, photons must reach reaction sites before their energy dissipates in less than one nanosecond. In photosynthetic processes, this is not possible. Because energy can exist in a superposition of states, it can travel all routes within a material at the same time. When a photon finds the correct destination, the superposition collapses, making the energy available. However, no purely quantum process can be wholly responsible, because some quantum processes slow down the movement of quantized objects through networks. Anderson localization prevents the spread of quantum states in random media. Because the state acts like a wave, it is vulnerable to disruptive interference effects. Another issue is the quantum zeno effect, in which an unstable state never changes if it is continuously measured/watched, because watching constantly nudges the state, preventing it from collapsing.[13][14]

Interactions between quantum states and the environment act like measurements. The classical interaction with the environment changes the wave-like nature of the quantum state just enough to prevent Anderson localisation, while the quantum zeno effect extends the quantum state's lifetime, allowing it to reach the reaction centre.[13] The proposed long lifetime of quantum coherence in the FMO influenced many scientists to investigate quantum coherence in the system, with Engel's 2007 paper being cited over 1500 times within 5 years of its publication. The proposal of Engel is still debated in literature with the suggestion that the original experiments were interpreted incorrectly assigning the spectral oscillations to electronic coherences instead of ground-state vibrational coherences, which will naturally be expected to live longer due to the narrower spectral width of vibrational transitions.

Computing

The problem of finding a reaction centre in a protein matrix is formally equivalent to many problems in computing. Mapping computing problems onto reaction center searches may allow light harvesting to work as a computational device, improving computational speeds at room temperature, yielding 100-1000x efficiency.[13]

References
  1. Tronrud, D.E.; Schmid, M.F.; Matthews, B.W. (April 1986). "Structure and X-ray amino acid sequence of a bacteriochlorophyll a protein from Prosthecochloris aestuarii refined at 1.9 A resolution". Journal of Molecular Biology. 188 (3): 443–54. doi:10.1016/0022-2836(86)90167-1. PMID 3735428.
  2. Fenna, R. E.; Matthews, B. W. (1975). "Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola". Nature. 258 (5536): 573–7. Bibcode:1975Natur.258..573F. doi:10.1038/258573a0. S2CID 35591234.
  3. Vulto, Simone I. E.; Neerken, Sieglinde; Louwe, Robert J. W.; De Baat, Michiel A.; Amesz, Jan; Aartsma, Thijs J. (1998). "Excited-State Structure and Dynamics in FMO Antenna Complexes from Photosynthetic Green Sulfur Bacteria". The Journal of Physical Chemistry B. 102 (51): 10630–5. doi:10.1021/jp983003v.
  4. Wendling, Markus; Przyjalgowski, Milosz A.; Gülen, Demet; Vulto, Simone I. E.; Aartsma, Thijs J.; Van Grondelle, Rienk van; Van Amerongen, Herbert van (2002). "The quantitative relationship between structure and polarized spectroscopy in the FMO complex of Prosthecochloris aestuarii: refining experiments and simulations". Photosynthesis Research. 71 (1–2): 99–123. doi:10.1023/A:1014947732165. PMID 16228505. S2CID 24164698.
  5. Pearlstein, Robert M. (1992). "Theory of the optical spectra of the bacteriochlorophyll an antenna protein trimer from Prosthecochloris aestuarii". Photosynthesis Research. 31 (3): 213–226. doi:10.1007/BF00035538. PMID 24408061. S2CID 22609422.
  6. Renger, Thomas [in German]; Marcus, R. A. (2002). "On the relation of protein dynamics and exciton relaxation in pigment–protein complexes: An estimation of the spectral density and a theory for the calculation of optical spectra" (PDF). The Journal of Chemical Physics. 116 (22): 9997–10019. Bibcode:2002JChPh.116.9997R. doi:10.1063/1.1470200.
  7. Rémigy, Hervé-W; Stahlberg, Henning; Fotiadis, Dimitrios; Müller, Shirley A; Wolpensinger, Bettina; Engel, Andreas; Hauska, Günter; Tsiotis, Georgios (July 1999). "The reaction center complex from the green sulfur bacterium Chlorobium tepidum: a structural analysis by scanning transmission electron microscopy". Journal of Molecular Biology. 290 (4): 851–8. doi:10.1006/jmbi.1999.2925. PMID 10398586.
  8. Rémigy, Hervé -W.; Hauska, Günter; Müller, Shirley A.; Tsiotis, Georgios (2002). "The reaction centre from green sulphur bacteria: progress towards structural elucidation". Photosynthesis Research. 71 (1–2): 91–8. doi:10.1023/A:1014963816574. PMID 16228504. S2CID 10285215.
  9. Adolphs, Julian; Renger, Thomas (October 2006). "How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria". Biophysical Journal. 91 (8): 2778–97. Bibcode:2006BpJ....91.2778A. doi:10.1529/biophysj.105.079483. PMC 1578489. PMID 16861264.
  10. Engel, Gregory S.; Calhoun, Tessa R.; Read, Elizabeth L.; Ahn, Tae-Kyu; Mancal, Tomáš; Cheng, Yuan-Chung; Blankenship, Robert E.; Fleming, Graham R. (2007). "Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems" (PDF). Nature. 446 (7137): 782–786. Bibcode:2007Natur.446..782E. doi:10.1038/nature05678. PMID 17429397. S2CID 13865546.
  11. Wilkins, David M.; Dattani, Nikesh S. (2015). "Why Quantum Coherence Is Not Important in the Fenna–Matthews–Olsen Complex". Journal of Chemical Theory and Computation. 11 (7): 3411–3419. arXiv:1411.3654. doi:10.1021/ct501066k. PMID 26575775. S2CID 15519516.
  12. R. Tempelaar; T. L. C. Jansen; J. Knoester (2014). "Vibrational Beatings Conceal Evidence of Electronic Coherence in the FMO Light-Harvesting Complex". J. Phys. Chem. B. 118 (45): 12865–12872. doi:10.1021/jp510074q. PMID 25321492.
  13. MIT (2013-11-25). "Quantum Light Harvesting Hints at Entirely New Form of Computing". Technologyreview.com. Retrieved 2013-12-06.
  14. Vattay, Gabor; Kauffman, Stuart A. (2013). "Evolutionary Design in Biological Quantum Computing". arXiv:1311.4688 [cond-mat.dis-nn].
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