Focus on quantum effects and noise in biomolecules

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Focus on quantum effects and noise in biomolecules
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2011 New J. Phys. 13 115002
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New Journal of Physics
The open–access journal for physics
EDITORIAL
Focus on quantum effects and noise in biomolecules
G R Fleming1,2 , S F Huelga3 and M B Plenio3,4
1
Department of Chemistry, University of California, Berkeley, CA 94720, USA
2
Physical Bioscience Division, Lawrence Berkeley National Laboratory,
Berkeley, CA 94720, USA
3
Institut für Theoretische Physik, Albert-Einstein Allee 11, Universität Ulm,
89069 Ulm, Germany
4
Quantum Optics and Laser Science Group, Blackett Laboratory,
Imperial College London, London SW7 2BW, UK
E-mail: [email protected], [email protected] and
[email protected]
New Journal of Physics 13 (2011) 115002 (5pp)
Received 15 August 2011
Published 4 November 2011
Online at http://www.njp.org/
doi:10.1088/1367-2630/13/11/115002
The role of quantum mechanics in biological organisms has
been a fundamental question of twentieth-century biology. It is only now,
however, with modern experimental techniques, that it is possible to observe
quantum mechanical effects in bio-molecular complexes directly. Indeed, recent
experiments have provided evidence that quantum effects such as wave-like
motion of excitonic energy flow, delocalization and entanglement can be seen
even in complex and noisy biological environments (Engel et al 2007 Nature
446 782; Collini et al 2010 Nature 463 644; Panitchayangkoon et al 2010 Proc.
Natl Acad. Sci. USA 107 12766). Motivated by these observations, theoretical
work has highlighted the importance of an interplay between environmental
noise and quantum coherence in such systems (Mohseni et al 2008 J. Chem.
Phys. 129 174106; Plenio and Huelga 2008 New J. Phys. 10 113019; OlayaCastro et al 2008 Phys. Rev. B 78 085115; Rebentrost et al 2009 New J. Phys.
11 033003; Caruso et al 2009 J. Chem. Phys. 131 105106; Ishizaki and Fleming
2009 J. Chem. Phys. 130 234111). All of this has led to a surge of interest in
the exploration of quantum effects in biological systems in order to understand
the possible relevance of non-trivial quantum features and to establish a potential
link between quantum coherence and biological function. These studies include
not only exciton transfer across light harvesting complexes, but also the avian
Abstract.
New Journal of Physics 13 (2011) 115002
1367-2630/11/115002+05$33.00
© IOP Publishing Ltd and Deutsche Physikalische Gesellschaft
2
compass (Ritz et al 2000 Biophys. J. 78 707), and the olfactory system (Turin
1996 Chem. Sens. 21 773; Chin et al 2010 New J. Phys. 12 065002).
These examples show that the full understanding of the dynamics at biomolecular length (10 Å) and timescales (sub picosecond) in noisy biological
systems can uncover novel phenomena and concepts and hence present a fertile
ground for truly multidisciplinary research.
The ‘quantum effects and noise in biomolecules’ focus issue, motivated by recent developments
concerning both experimental and theoretical aspects, collects a select list of research results
that explore from a variety of angles the question of whether quantum effects exist in biological
systems and, if they do, what possible functional role quantum effects may play.
Thanks to pioneering experiments on exciton transfer [1–3] and subsequent theoretical
work linking environmental noise and quantum coherence [4–9], the exploration of this
interplay in photosynthetic complexes and the development of relevant spectroscopic techniques
represent an emphasis of current research. On the theoretical side, this focus issue reports the
work of [13], which explores the detailed mechanisms that underly noise-assisted transport
further and applies these to the Fenna–Matthew–Olson (FMO) complex to explain how noise
alters the pathways of energy transfer across the complex, suppressing ineffective pathways
and facilitating direct ones to the reaction center. Building on this, detailed studies of the
external parameters that help maximize the efficiency [14] can then be carried out and
understood.
While Chin et al [13] and previous work [4–9] suggests that the fundamental mechanisms
underpinning noise-assisted transport are robust, the specific details of the exciton–phonon
coupling may result in variations of dynamical features. Indeed, it is expected that the nature of
the environmental correlations does play a significant role in the dynamics of the excitation
energy transport. In [15], for example, a model for bath-induced electronic transitions is
developed and then applied to study the dynamics of electronic dephasing in the FMO complex
using two-dimensional Fourier transform electronic spectroscopy. This paper provides evidence
that the protein matrix protects coherences by globally correlating fluctuations in transition
energies and that the lifetimes of individual coherences are distinct, thus suggesting that the
FMO complex has been locally tuned by natural selection to optimize transfer efficiency
by exploiting quantum coherence. The effect of spatial correlations on quantum coherent
bio-molecular energy transfer is also investigated in detailed and numerically exact studies
in [16], where it is shown in a simple toy model of a single donor–acceptor pair that quantum
coherent transfer of excitations between bio-molecular chromophores is strongly influenced
by spatial correlations of environmental fluctuations. Hossein-Nejad and Scholes [17] study
analytically the dynamics of energy transfer and dephasing in a molecular dimer with degenerate
energies interacting with an anti-correlated, collective vibrational bath and find that, under the
influence of a collective phonon bath, coherence survives longer in systems with weak electronic
couplings. Correlated fluctuations may also play a role in the exciton dynamics and spectroscopy
of DNA, which is in turn of relevance for an understanding of photodamage (Dijkstra and
Tanimura [18]). It also noted in this focus issue that the transport dynamics in networks will
not only be affected by dephasing noise, but also by oscillatory perturbations which may lead
to enhancement or strong suppression of transport, as in [19, 20].
New Journal of Physics 13 (2011) 115002 (http://www.njp.org/)
3
The energy transfer dynamics in a photosynthetic membrane is another example of
current interest that is studied in this focus issue. Empirical findings of an illumination-driven
transition in the bio-molecular membrane architecture of the purple bacteria Rhodospirillum
photometricum are the motivation for studies of the interplay between excitation kinetics and
reaction-center dynamics in purple bacteria reported in [21]. It is suggested that the shift in
preferred architectures can be traced back to the interplay between the excitation kinetics and
the reaction center dynamics. The net effect is that the bacteria profit from efficient metabolism
at low illumination intensities while using dissipation to avoid an oversupply of energy at high
illumination intensities. Such findings might depend sensitively on the specifics of the modeling
of the system–environment coupling. Hsin et al [22] in turn provide evidence to the contrary in
an examination of the excitation transfer dynamics in a single RCLH1PufX core complex dimer
and show that the generalized Förster theory provides accurate transfer rates.
The mounting evidence of electronic coherence during excitation energy transfer in
photosynthetic antenna complexes has reinvigorated the discussion concerning the role that
coherence and entanglement may play in the functionality of these molecular systems. These
issues are explored in several papers in this focus issue. The study reported in [23] aims
to establish quantitative relationships between the yield of a light-harvesting complex and
the distribution of entanglement among its components in the FMO complex and finds that
there is an inverse relationship between the quantum efficiency and the average entanglement
between distant donor sites. Ishizaki and Fleming [24] explores the quantum entanglement
among the chlorophyll molecules in light-harvesting complex II (LHII) and find robust
quantum entanglement under physiological conditions for the case of a single elementary
excitation. However, spectroscopically detectable delocalized states are entangled states as long
as one follows the formal definition of quantum entanglement, and the benefit of considering
entanglement measures lies in their potential to more accurately characterize delocalized
states [25]. The role of the method of excitation is discussed in [26], and this continues to
be subject to lively debate.
One might speculate that the presence of entanglement in light-harvesting complexes may
be used to achieve a speed-up analogous to those found in quantum algorithms. To decide this
question, Hoyer et al [27] compares the dynamics in light-harvesting systems to the dynamics
of quantum walks. For the FMO complex they find that while there is indeed speed-up at short
times, it is short lived (70 fs) and hence negligible compared to the total transfer time and longlived quantum coherences that extend to pico-second timescales. These results suggest that
quantum coherent effects in biological systems might be optimized for efficiency or robustness,
but not for a possible quantum speed-up [28]. Notably, though, the situation might change in
assemblies of, for example, nano-engineered light-harvesting complexes. Indeed, Lloyd and
Mohseni [29] suggests that symmetry-enhanced supertransfer of delocalized quantum states
might enhance the speed and distance across which energy transfer is possible and may play a
role in recent observations of anomalously long diffusion lengths in nano-engineered assembly
of light-harvesting complexes [30].
The previous examples were mostly concerned with electronic coherence, but vibrational
coherence is also of interest. Indeed, in carotenoids of the LHII complex two-color vibronic
coherence spectroscopy can be used to observe long-lived vibrational coherences in the ground
electronic state of carotenoid molecules, with decoherence times in excess of 1 ps, as reported
in [31]. Here, it is also observed that the vibrational coherence time increases significantly
New Journal of Physics 13 (2011) 115002 (http://www.njp.org/)
4
for the carotenoid in the complex, providing further support to suggestions that long-lived
electronic coherences in light-harvesting complexes are facilitated by correlated motion of
the chromophores and surrounding proteins. Vibrational energy flow may also be affected by
quantum effects, which may lead to localization and hence influence biomolecule function,
including control of reaction kinetics. The authors of [32] studied these effects and find that
simplified treatments based on golden-rule calculations often overestimate the mode-damping
rate.
The interplay between theory and experiment will benefit not only from improved
theoretical methods and questions, but also depends on the development of more sensitive
experimental methods. More information may be extracted, for instance with the help of higher
order spectroscopic techniques such as fifth-order two-dimensional electronic spectroscopy.
Non-perturbative calculations, for example, show clear patterns that correspond to the electronic
structure of one- and two-exciton manifolds of a FMO light-harvesting complex [33]. As
reported in [34], the incorporation of the effects of three-exciton correlations in the simulation
of population and coherence relaxation dynamics also induces new peaks that are absent or
much weaker when the three-exciton variables are factorized and thus aid the interpretation
of observations in a recent experiment [1]. In these investigations the response functions are
computed from effective equations that neglect the detailed atomistic structure of the systems.
Jeon and Cho [35] examine the extent to which a refined and accurate picture is computationally
feasible. They present a new computational method that calculates nonlinear response
function in the classical limit from a series of classical molecular dynamics simulations,
employing a quantum mechanical/molecular mechanical force field and applying it to the twodimensional IR spectroscopy of carbon monoxide and N-methylacetamide, each solvated in a
water cluster.
While excitation energy transport concerns very light quasi-particles, such as excitons,
biological systems also depend crucially on the transport of heavier species such as protons to
support, for example, proton transfer reactions in enzymes or even ion channels that regulate
the flow of particular ions across the cell membrane and are important in a variety of processes,
including neuronal communications. Indeed, Bothma et al [36] explore the role of quantum
effects in proton transfer reactions in enzymes and examine in some detail whether quantum
tunneling can play a role in noisy environments. Vaziri and Plenio [20] explore the related
question of whether quantum coherence may exist and play a functional a role in the properties
of the selectivity filter of ion channels such as the potassium channel, and they propose several
experimental procedures to test this hypothesis.
This issue also reports work on a variety of other topics, including the exploration of the
quantization of conformational changes in α-helical proteins [37] and the exploration of an
intricate interplay between the quantum Zeno effect and the coherent excitation of radical-ion
pairs, which is proposed in [38] to lead to a high angular sensitivity of radical pair reactions,
and might be of relevance for the avian compass.
In summary, this focus issue of New Journal of Physics presents a series of complementary
analyses of the rich interplay between quantum coherence and decoherence in a wide variety
of systems of biological relevance during an interesting period of active research and rapid
development. The whole picture is still far from complete and we anticipate that exciting
developments lie ahead.
New Journal of Physics 13 (2011) 115002 (http://www.njp.org/)
5
References
[1] Engel G R, Calhoun T R, Read E L, Ahn T K, Mančal T, Cheng Y C, Blankenship R E and Fleming G R
2007 Nature 446 782
[2] Collini E, Wong C Y, Wilk K E, Curmi P M G, Brumer P and Scholes G D 2010 Coherently wired
light-harvesting in photosynthetic marine algae at ambient temperature Nature 463 644
[3] Panitchayangkoon G, Hayes D, Fransted K A, Caram J R, Harel E, Wen J, Blankenship R E and Engel G S
2010 Proc. Natl Acad. Sci. USA 107 12766
[4] Mohseni M, Rebentrost P, Lloyd S and Aspuru-Guzik A 2008 J. Chem. Phys. 129 174106
[5] Plenio M B and Huelga S F 2008 New J. Phys. 10 113019
[6] Olaya-Castro A, Lee C-F, Fassioli-Olsen F and Johnson N F 2008 Phys. Rev. B 78 085115
[7] Rebentrost P, Mohseni M, Kassal I, Lloyd S and Aspuru-Guzik A 2009 New J. Phys. 11 033003
[8] Caruso F, Chin A W, Datta A, Huelga S F and Plenio M B 2009 J. Chem. Phys. 131 105106
[9] Ishizaki A and Fleming G R 2009 J. Chem. Phys. 130 234111
[10] Ritz T, Adem S and Schulten K 2000 Biophys. J. 78 707
[11] Turin L 1996 Chem. Sens. 21 773
[12] Brookes J C, Hartoutsiou F, Horsfield A P and Stoneham A M 2007 Phys. Rev. Lett. 98 038101
[13] Chin A W, Datta A, Caruso F, Huelga S F and Plenio M B 2010 New J. Phys. 12 065002
[14] Wu J, Liu F, Shen Y, Cao J and Silbey R J 2010 New J. Phys. 12 105012
[15] Hayes D, Panitchayangkoon G, Fransted K A, Caram J R, Wen J, Freed K F and Engel G S 2010 New J. Phys.
12 065042
[16] Nalbach P, Eckel J and Thorwart M 2010 New J. Phys. 12 065043
[17] Hossein-Nejad H and Scholes G D 2010 New J. Phys. 12 065045
[18] Dijkstra A G and Tanimura Y 2010 New J. Phys. 12 055005
[19] Asadian A, Tiersch M, Guerreschi G G, Cai J, Popescu S and Briegel H J 2010 New J. Phys. 12 075019
[20] Vaziri A and Plenio M B 2010 New J. Phys. 12 085001
[21] Caycedo-Soler F, Rodrı́guez F J, Quiroga L and Johnson N F 2010 New J. Phys. 12 095008
[22] Hsin J, Strümpfer J, Sener M, Qian P, Hunter C N and Schulten K 2010 New J. Phys. 12 085005
[23] Fassioli F and Olaya-Castro A 2010 New J. Phys. 12 085006
[24] Ishizaki A and Fleming G R 2010 New J. Phys. 12 055004
[25] Ishizaki A and Fleming G R 2012 Ann. Rev. Cond. Matt. Phys. at press (doi:10.1146/annurev-conmatphys020911-125126)
[26] Mančal T and Valkunas L 2010 New J. Phys. 12 065044
[27] Hoyer S, Sarovar M and Whaley K B 2010 New J. Phys. 12 065041
[28] Ishizaki A and Fleming G R 2009 Proc. Natl Acad. Sci. USA 106 17255
[29] Lloyd S and Mohseni M 2010 New J. Phys. 12 075020
[30] Escalante M, Lenferink A, Zhao Y, Tas N, Huskens J, Hunter C N, Subramaniam V and Otto C 2010 Nano
Lett. 10 1450
[31] Davis J A, Cannon E, Van Dao L, Hannaford P, Quiney H M and Nugent K A 2010 New J. Phys. 12 085015
[32] Leitner D M 2010 New J. Phys. 12 085004
[33] Brüggemann B and Pullerits T 2011 New J. Phys. 13 025024
[34] Yang L, Abramavicius D and Mukamel S 2010 New J. Phys. 12 065046
[35] Jeon J and Cho M 2010 New J. Phys. 12 065001
[36] Bothma J P, Gilmore J B and McKenzie R H 2010 New J. Phys. 12 055002
[37] Atanasov V and Omar Y 2010 New J. Phys. 12 055003
[38] Katsoprinakis G E, Dellis A T and Kominis I K 2010 New J. Phys. 12 085016
New Journal of Physics 13 (2011) 115002 (http://www.njp.org/)