Photosynthetic Vesicle Architecture and Constraints on Efficient Energy Harvesting

Sener, Melih; Strümpfer, Johan; Timney, John A.; Freiberg, Arvi; Hunter, C. Neil; Schulten, Klaus

doi:10.1016/j.bpj.2010.04.013

Cited by 63 publications

(133 citation statements)

References 81 publications

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“…Excitation transfer kinetics in the chromatophore was reported experimentally in (Woodbury and Parson, 1984;Visscher et al, 1989;Crielaard et al, 1994;Hess et al, 1994Hess et al, , 1995. Exciton migration across the network of light harvesting complexes in the chromatophore can be described by a rate matrix K which is constructed from inter-complex exciton transfer rates k IJ , the latter given by Equation (S6), as follows (Sener et al, 2010(Sener et al, , 2007 …”

Section: Stage I: Light Absorption Excitation Energy Transfer and Qmentioning

confidence: 99%

“…and Novoderezhkin, 2006b;Strümpfer andSchulten, 2011, 2012a) methods. The chromatophore exhibits also the features of modularity, repair, and assembly of components (Hsin et al, 2010a), high quantum yield of organelle-scale pigment networks (Ş ener et al, 2007, 2010Cartron et al, 2014), isolation of the electron transfer chains (Ş ener and Schulten, 2008), co-accommodation of competing functions such as efficient energy transfer and diffusion in the quinone/quinol pool Sener et al, 2010), as well as adaptation to changing external conditions (Adams and Hunter, 2012;Woronowicz et al, 2011a;Niederman, 2013;Woronowicz et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Overall energy conversion efficiency of a photosynthetic vesicle

Sener

Strümpfer

Singharoy

et al. 2016

eLife

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174

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The chromatophore of purple bacteria is an intracellular spherical vesicle that exists in numerous copies in the cell and that efficiently converts sunlight into ATP synthesis, operating typically under low light conditions. Building on an atomic-level structural model of a low-lightadapted chromatophore vesicle from Rhodobacter sphaeroides, we investigate the cooperation between more than a hundred protein complexes in the vesicle. The steady-state ATP production rate as a function of incident light intensity is determined after identifying quinol turnover at the cytochrome bc 1 complex (cytbc 1 ) as rate limiting and assuming that the quinone/quinol pool of about 900 molecules acts in a quasi-stationary state. For an illumination condition equivalent to 1% of full sunlight, the vesicle exhibits an ATP production rate of 82 ATP molecules/s. The energy conversion efficiency of ATP synthesis at illuminations corresponding to 1%-5% of full sunlight is calculated to be 0.12-0.04, respectively. The vesicle stoichiometry, evolutionarily adapted to the low light intensities in the habitat of purple bacteria, is suboptimal for steady-state ATP turnover for the benefit of protection against over-illumination.

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Section: Stage I: Light Absorption Excitation Energy Transfer and Qmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Overall energy conversion efficiency of a photosynthetic vesicle

Sener

Strümpfer

Singharoy

et al. 2016

eLife

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174

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“…We describe this approach through its application to the strikingly symmetric antenna complexes of purple bacteria [16], which feature tightly packed bacteriochlorophylls and considerable excitonic delocalization [17][18][19][20][21][22][23][24][25][26][27][28]. This delocalization is known to give rise to supertransfer, in particular for EET within the LH2 complex [29][30][31].…”

mentioning

confidence: 99%

Distinguishing the roles of energy funnelling and delocalization in photosynthetic light harvesting

Baghbanzadeh

Kassal

2016

Phys. Chem. Chem. Phys.

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Photosynthetic complexes improve the transfer of excitation energy from peripheral antennas to reaction centers in several ways. In particular, a downward energy funnel can direct excitons in the right direction, while coherent excitonic delocalization can enhance transfer rates through the cooperative phenomenon of supertransfer. However, isolating the role of purely coherent effects is difficult because any change to the delocalization also changes the energy landscape. Here, we show that the relative importance of the two processes can be determined by comparing the natural light-harvesting apparatus with counterfactual models in which the delocalization and the energy landscape are altered. Applied to the example of purple bacteria, our approach shows that although supertransfer does enhance the rates somewhat, the energetic funnelling plays the decisive role. Because delocalization has a minor role (and is sometimes detrimental), it is most likely not adaptive, being a side-effect of the dense chlorophyll packing that evolved to increase light absorption per reaction center.Photosynthetic organisms harvest light using antenna complexes containing many chlorophyll molecules [1]. The energy collected by the antennas is then transmitted, through excitonic energy transfer (EET) [2], to a reaction center (RC), where it drives the first chemical reactions of photosynthesis. The thorough study of EET in photosynthetic antennas has been motivated, in part, by the prospect of learning how to design more efficient artificial light-harvesting devices [3,4].It has long been recognized that excitons in many photosynthetic complexes are directed toward the RC energetically: if the antennas lie higher in energy than the RC, the excitons can spontaneously funnel to the RC. A more recent discovery is that coherent mechanisms can also enhance light-harvesting efficiency. In particular, excitonic eigenstates may be localized or delocalized over a number of molecules, depending on the strength of their couplings [2,[5][6][7][8]. Delocalization-i.e., coherence in the site basis-makes the aggregate behave differently than a single chlorophyll molecule, and phenomena such as superradiance [9,10], superabsorption [11], and supertransfer [12][13][14][15] can occur in densely packed aggregates. Specifically, supertransfer occurs when delocalization in the donor and/or the acceptor enhances the rate of the (incoherent) EET between them.The presence of both funnelling and supertransfer suggests that their contributions to the efficiency could be quantified. However, the two effects are too closely related for such a separation to be easily carried out; in particular, a change to the extent of delocalization requires changing excitonic couplings, which also determine the energy landscape. In other words, because delocalization and the energy landscape are intimately connected, it is not sufficient to alter one property to see what happens to the efficiency, because doing so also alters the other property as well.Here, we show that the ...

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“…46,47 The close proximity of LH1 and RC brings into question whether excitation transfer occurs incoherently between them, as has been previously assumed, but to be expected only for transfer between distant groups of pigments. [48][49][50] By using the HEOM the assumption's validity can be tested.…”

Section: Introductionmentioning

confidence: 99%

Excited state dynamics in photosynthetic reaction center and light harvesting complex 1

Strümpfer

Schulten

2012

The Journal of Chemical Physics

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Key to efficient harvesting of sunlight in photosynthesis is the first energy conversion process in which electronic excitation establishes a trans-membrane charge gradient. This conversion is accomplished by the photosynthetic reaction center (RC) that is, in case of the purple photosynthetic bacterium Rhodobacter sphaeroides studied here, surrounded by light harvesting complex 1 (LH1). The RC employs six pigment molecules to initiate the conversion: four bacteriochlorophylls and two bacteriopheophytins. The excited states of these pigments interact very strongly and are simultaneously influenced by the surrounding thermal protein environment. Likewise, LH1 employs 32 bacteriochlorophylls influenced in their excited state dynamics by strong interaction between the pigments and by interaction with the protein environment. Modeling the excited state dynamics in the RC as well as in LH1 requires theoretical methods, which account for both pigment-pigment interaction and pigment-environment interaction. In the present study we describe the excitation dynamics within a RC and excitation transfer between light harvesting complex 1 (LH1) and RC, employing the hierarchical equation of motion method. For this purpose a set of model parameters that reproduce RC as well as LH1 spectra and observed oscillatory excitation dynamics in the RC is suggested. We find that the environment has a significant effect on LH1-RC excitation transfer and that excitation transfers incoherently between LH1 and RC.

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Photosynthetic Vesicle Architecture and Constraints on Efficient Energy Harvesting

Cited by 63 publications

References 81 publications

Overall energy conversion efficiency of a photosynthetic vesicle

Overall energy conversion efficiency of a photosynthetic vesicle

Distinguishing the roles of energy funnelling and delocalization in photosynthetic light harvesting

Excited state dynamics in photosynthetic reaction center and light harvesting complex 1

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