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Dynamics and Mechanism of Short-Range Electron Transfer Reactions in Flavoproteins.

Kundu, Mainak
http://rave.ohiolink.edu/etdc/view?acc_num=osu1557100528978923

Abstract Details

2019, Doctor of Philosophy, Ohio State University, Chemistry.
Short-range electron transfer (ET) reactions are extensively used in light perception processes in flavoproteins. Such reactions an ultrafast and occur on the similar timescales as local protein-solvent fluctuations from femtoseconds to picoseconds and thus the two dynamics are expected to be coupled. Using the model protein of flavodoxin in its semiquinone state, we systematically characterized the photoinduced redox cycle of charge separation and charge recombination with mutations of different aromatic electron donors (tryptophan and tyrosine) and local residues to change the redox properties. We observed the ET dynamics in a few picoseconds, strongly following a stretched behavior resulting from a coupling between local environment fluctuations and these ET processes. We further observed the hot vibrational-state formation through charge recombination and the subsequent cooling dynamics and both processes are also in a few picoseconds. Combined with our previous studies of femtosecond ET in oxidized flavodoxin, these results coherently reveal the evolution of the ET dynamics from single to stretched exponential behaviors and elucidate the coupling mechanism. The observed hot vibration-state formation is robust and general and should be considered in all photoinduced back ET processes in flavoproteins. To analyze the role of tunneling distances in such reactions, we determined ET dynamics in a flavin–tryptophan pair at distances ranging from 3.2 to 18 Å, in 10 flavodoxin mutants with constant driving forces. We widely observed the stretched ET behavior with coupling from local solvation processes, and heterogenous ET dynamics from the large fluctuations (0.4 to 0.8 Å) in W donors located in flexible loop regions. We further observed the exponentially correlated distance–dependent ET severely impacted by local protein structures. At short distances, ET is highly favored by overlapping orbital interactions. At longer separation, tunneling pathways may uniquely differ within a protein and alter tunneling barriers to change the ET dynamics. Slow ET dynamics at long distances leads to energy loss via triplet dynamics, consistent with lower reaction yields. These results reveal how donor–acceptor configurations control ET mechanisms and signal transduction in photoreceptors. The accelerated growth in Oryza Sativa by the trimeric protein OsHAl3 is regulated by blue light through an unknown mechanism. We identified a photoreduction of the chromophore FMN from electron donors W79 and W82 on blue light illumination. At the active site, we obtained solvation dynamics in the ET-inert mutant in 1.9 ps (20%), 16 ps (42%), and 480 ps (37%), with the large energy relaxation of 217 cm-1, thus revealing a water-exposed FMN environment. We identified ultrafast forward ET and back ET dynamics in 1.2 ps, β=0.92 and 0.6 ps, β=0.97 for the donor W79. For W82, we resolved a faster forward ET and a slower back ET reaction in 4.0 ps, β=0.96 and 0.41 ps, β=1.0, respectively. With faster formation and longer recombination dynamics, W82 is the main electron donor, and the charge-separated intermediate could be key to downstream signaling. The large β values indicate minor ET coupling with solvent motions due to the slower environmental relaxations. We also observed formation of vibrationally hot BET product, consistent with the flavodoxin ET processes. These ET dynamics are essential for the blue light perception and is the primary event for signal transduction. For the special mutant C119S, we observed ET dynamics comparable to the wild-type, indicating absence of C119–C125 disulfide bond, in contrast to the light--inactive homolog AtHAL3. Together with the observation of C119-C125 disulfide bond in light structure of OsHAL3, the cysteines are possibly responsible for light induced structural changes.
Dongping Zhong, Dr. (Advisor)
Heather Allen, Dr. (Committee Member)
Sherwin Singer, Dr. (Committee Member)
120 p.
Chemistry
Flavoproteins; Ultrafast electron transfer; Nonequilibrium protein dynamics

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Citations

  • Kundu, M. (2019). Dynamics and Mechanism of Short-Range Electron Transfer Reactions in Flavoproteins. [Doctoral dissertation, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1557100528978923

    APA Style (7th edition)

  • Kundu, Mainak. Dynamics and Mechanism of Short-Range Electron Transfer Reactions in Flavoproteins. 2019. Ohio State University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1557100528978923.

    MLA Style (8th edition)

  • Kundu, Mainak. "Dynamics and Mechanism of Short-Range Electron Transfer Reactions in Flavoproteins." Doctoral dissertation, Ohio State University, 2019. http://rave.ohiolink.edu/etdc/view?acc_num=osu1557100528978923

    Chicago Manual of Style (17th edition)

osu1557100528978923
203
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This open access ETD is published by The Ohio State University and OhioLINK.