Protein dynamics to optimize and control bacterial photosynthesis

LeBard, David N.; Martin, Daniel R.; Lin, Su; Woodbury, Neal W.; Matyushov, Dmitry V.

doi:10.1039/c3sc51327k

Cited by 24 publications

(56 citation statements)

References 83 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…ET reactions in the purple bacterial photosynthetic RCs (PBRCs) have been by far the most widely studied (28), and it is primarily in connection with this system that the idea of invertedregion ET is considered (15,16). However, in PBRCs the primary radical pair recombination reaction (so-called P + H L − recombination), at least for the native or wild-type (WT) system, is known not to occur in the inverted region (29)(30)(31)(32). In fact, the unproductive P + H L − recombination reaction in WT PBRCs is nearly activationless (33).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

Makita

Hastings

2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

In all photosynthetic organisms, light energy is used to drive electrons from a donor chlorophyll species via a series of acceptors across a biological membrane. These light-induced electron-transfer processes display a remarkably high quantum efficiency, indicating a near-complete inhibition of unproductive charge recombination reactions. It has been suggested that unproductive charge recombination could be inhibited if the reaction occurs in the so-called inverted region. However, inverted-region electron transfer has never been demonstrated in any native photosynthetic system. Here we demonstrate that the unproductive charge recombination in native photosystem I photosynthetic reaction centers does occur in the inverted region, at both room and cryogenic temperatures. Computational modeling of light-induced electron-transfer processes in photosystem I demonstrate a marked decrease in photosynthetic quantum efficiency, from 98% to below 72%, if the unproductive charge recombination process does not occur in the inverted region. Inverted-region electron transfer is therefore demonstrated to be an important mechanism contributing to efficient solar energy conversion in photosystem I. Inverted-region electron transfer does not appear to be an important mechanism in other photosystems; it is likely because of the highly reducing nature of photosystem I, and the energetic requirements placed on the pigments to operate in such a regime, that the inverted-region electron transfer mechanism becomes important.

show abstract

Section: Discussionmentioning

confidence: 99%

“…In fact, the unproductive P + H L − recombination reaction in WT PBRCs is nearly activationless (33). In PBRCs it appears to be the case that mechanisms related to protein relaxations in response to ET are (more) important in maximizing photosynthetic efficiency (29)(30)(31)(32).…”

Section: Discussionmentioning

confidence: 99%

Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

Makita

Hastings

2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…In order to illustrate how actual calculations are performed, we start with the loss spectrum χ ′′ X (ω) (figure 4) of the energy gap fluctuations in the bacterial reaction center [40]. The loss function is calculated from the time autocorrelation function .…”

Section: Gibbs Ensemble Broken Ergodicity and Gaussian Fluctuationsmentioning

confidence: 99%

“…The loss function is calculated from the time autocorrelation function . The reaction is studied by MD simulations of the wild-type reaction center of Rhodobacter sphaeroides [40]. The loss function χ ′′ X (ν) is plotted vs ν = ω/(2π).…”

Section: Gibbs Ensemble Broken Ergodicity and Gaussian Fluctuationsmentioning

confidence: 99%

Protein electron transfer: is biology (thermo)dynamic?

Matyushov

2015

J. Phys.: Condens. Matter

140

View full text Add to dashboard Cite

Simple physical mechanisms are behind the flow of energy in all forms of life. Energy comes to living systems through electrons occupying high-energy states, either from food (respiratory chains) or from light (photosynthesis). This energy is transformed into the cross-membrane proton-motive force that eventually drives all biochemistry of the cell. Life's ability to transfer electrons over large distances with nearly zero loss of free energy is puzzling and has not been accomplished in synthetic systems. The focus of this review is on how this energetic efficiency is realized. General physical mechanisms and interactions that allow proteins to fold into compact water-soluble structures are also responsible for a rugged landscape of energy states and a broad distribution of relaxation times. Specific to a protein as a fluctuating thermal bath is the protein-water interface, which is heterogeneous both dynamically and structurally. The spectrum of interfacial fluctuations is a consequence of protein's elastic flexibility combined with a high density of surface charges polarizing water dipoles into surface nanodomains. Electrostatics is critical to the protein function and the relevant questions are: (i) What is the spectrum of interfacial electrostatic fluctuations? (ii) Does the interfacial biological water produce electrostatic signatures specific to proteins? (iii) How is protein-mediated chemistry affected by electrostatics? These questions connect the fluctuation spectrum to the dynamical control of chemical reactivity, i.e. the dependence of the activation free energy of the reaction on the dynamics of the bath. Ergodicity is often broken in protein-driven reactions and thermodynamic free energies become irrelevant. Continuous ergodicity breaking in a dense spectrum of relaxation times requires using dynamically restricted ensembles to calculate statistical averages. When applied to the calculation of the rates, this formalism leads to the nonergodic activated kinetics, which extends the transition-state theory to dynamically dispersive media. Releasing the grip of thermodynamics in kinetic calculations through nonergodicity provides the mechanism for an efficient optimization between reaction rates and the spectrum of relaxation times of the protein-water thermal bath. Bath dynamics, it appears, play as important role as the free energy in optimizing biology's performance.

show abstract

“…These examples illustrate that the hierarchically organized mobility of proteins is conferred by their structure and by the order and local arrangement of amino acids with different space requirements and chemical functions [99]. Despite the pure sequence-dependent intramolecular mobility, the sensitivity of molecular mobility from the environmental conditions is also determined by the inclusion of certain amino acids at certain positions in the peptide sequence.…”

Section: Limited Mobilitymentioning

confidence: 98%

What are proteins teaching us on fundamental strategies for molecular nanotechnology?

Koehler

2015

Nanotechnology Reviews

View full text Add to dashboard Cite

Besides the fundamental competition between the top-down and bottom-up approaches in nanotechnology, there are some basic aspects for organizing structures and functions at the molecular level. The recent challenges to the development of nanotechnology are marked by a group of general requirements: selection of suited building units, overcoming the restrictions of planar technology, shrinking of nanofabrication facilities, sustainable production and management of life cycles, organization of autonomy and communication at the nano-level, and the optimization of power consumption and energy management. Looking at the natural principles in the construction, synthesis, and function of proteins helps in understanding the principal differences between the currently applied technologies and the characteristics of biomolecular mechanisms in cells. This view allows formulating seven basic rules to meet the general requirements for future developments in molecular nanotechnology.

show abstract

Protein dynamics to optimize and control bacterial photosynthesis

Cited by 24 publications

References 83 publications

Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

Inverted-region electron transfer as a mechanism for enhancing photosynthetic solar energy conversion efficiency

Protein electron transfer: is biology (thermo)dynamic?

What are proteins teaching us on fundamental strategies for molecular nanotechnology?

Contact Info

Product

Resources

About