news & views PROTON-COUPLED ELECTRON TRANSFER
Free radicals under control
Biological solar energy conversion requires the coordinated and rapid movement of protons and electrons through complex proteins, called reaction centres. Now, an artificial and structurally simple reaction centre has been synthesized that mimics an important, photosynthetic charge relay.
Bridgette A. Barry
I
n many biological reactions, electrons must be transferred from point to point over a long distance. In proteins, this transfer is mediated by quantum tunnelling, with a rate that falls off exponentially with distance1. Accelerating this process — into a physiologically relevant time regime — is the job of redox-active cofactors, which are typically embedded into the protein matrix 2. These cofactors are transiently oxidized and reduced and define a radical transport pathway that operates by multistep tunnelling. In some proteins, these radical intermediates are directly detectable using spectroscopic techniques such as electron paramagnetic resonance (EPR); therefore researchers are beginning to better understand the complexity of these processes. An important aromatic amino acid in electron transfer in biology is tyrosine, which serves as an intrinsic electrontransfer intermediate in photosynthesis and DNA synthesis (reviewed in ref. 3). In solution, tyrosyl free-radicals can be generated by photolysis4 but they are very reactive and quickly decay. Therefore, biology has evolved methods of using these a
free radicals in catalysis, extending their lifetime and preventing unwanted side reactions. Exquisite control mechanisms are used to move the unpaired electron rapidly, harness available free energy, and control the direction of electron transfer. However, these control mechanisms are not well understood. Now, writing in Nature Chemistry, Ana Moore and colleagues provide5 new insight into this complicated chemistry by synthesizing and studying an artificial, simplified reaction centre. This designed system mimics a charge relay that is important in photosynthesis. A prototypical example of tyrosine-based radical transfer occurs in the photosynthetic reaction centre, photosystem II. This system carries out the light-driven oxidation of water and subsequently passes the acquired electrons on to an acceptor called plastoquinone. The reduced and protonated form of the quinone functions as a mobile carrier in the photosynthetic thylakoid membrane. Photosystem II is a large complex enzyme that contains at least 20 protein subunits and multiple redoxactive cofactors (Fig. 1)6; however, much progress has been made in understanding
how it works. We know that an initial photoexcitation of chlorophyll generates a charge-separated state in which a quinone acceptor is reduced and a Mn4CaO5 cluster is oxidized. This reaction occurs across the thylakoid membrane and is mediated by a chain of redox-active groups, including chlorophyll, pheophytin and a redox-active tyrosine, called YZ, which is tyrosine 161 of a subunit called D1. YZ mediates radical transfer between the primary chlorophyll donor, P680+, and the metal cluster, at which oxygen is generated from water. This metal cluster or oxygen-evolving complex (OEC) accumulates four oxidizing equivalents, with YZ functioning as the relay on each event. Photosystem II also contains another redox-active tyrosine, YD, which is tyrosine 160 of the subunit called D2. It differs from YZ in that it is not required for oxygen evolution, has a lower potential, and forms a relatively stable radical. As shown in the X-ray structure of Umena et al. (Fig. 1)6, each of these redox-active tyrosines is predicted to hydrogen bond to a histidine. The placement of bound water molecules and proximity to the Mn4CaO5 cluster distinguish YD and
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Free radicals under control
Biological solar energy conversion requires the coordinated and rapid movement of protons and electrons through complex proteins, called reaction centres. Now, an artificial and structurally simple reaction centre has been synthesized that mimics an important, photosynthetic charge relay.
Bridgette A. Barry
I
n many biological reactions, electrons must be transferred from point to point over a long distance. In proteins, this transfer is mediated by quantum tunnelling, with a rate that falls off exponentially with distance1. Accelerating this process — into a physiologically relevant time regime — is the job of redox-active cofactors, which are typically embedded into the protein matrix 2. These cofactors are transiently oxidized and reduced and define a radical transport pathway that operates by multistep tunnelling. In some proteins, these radical intermediates are directly detectable using spectroscopic techniques such as electron paramagnetic resonance (EPR); therefore researchers are beginning to better understand the complexity of these processes. An important aromatic amino acid in electron transfer in biology is tyrosine, which serves as an intrinsic electrontransfer intermediate in photosynthesis and DNA synthesis (reviewed in ref. 3). In solution, tyrosyl free-radicals can be generated by photolysis4 but they are very reactive and quickly decay. Therefore, biology has evolved methods of using these a
free radicals in catalysis, extending their lifetime and preventing unwanted side reactions. Exquisite control mechanisms are used to move the unpaired electron rapidly, harness available free energy, and control the direction of electron transfer. However, these control mechanisms are not well understood. Now, writing in Nature Chemistry, Ana Moore and colleagues provide5 new insight into this complicated chemistry by synthesizing and studying an artificial, simplified reaction centre. This designed system mimics a charge relay that is important in photosynthesis. A prototypical example of tyrosine-based radical transfer occurs in the photosynthetic reaction centre, photosystem II. This system carries out the light-driven oxidation of water and subsequently passes the acquired electrons on to an acceptor called plastoquinone. The reduced and protonated form of the quinone functions as a mobile carrier in the photosynthetic thylakoid membrane. Photosystem II is a large complex enzyme that contains at least 20 protein subunits and multiple redoxactive cofactors (Fig. 1)6; however, much progress has been made in understanding
how it works. We know that an initial photoexcitation of chlorophyll generates a charge-separated state in which a quinone acceptor is reduced and a Mn4CaO5 cluster is oxidized. This reaction occurs across the thylakoid membrane and is mediated by a chain of redox-active groups, including chlorophyll, pheophytin and a redox-active tyrosine, called YZ, which is tyrosine 161 of a subunit called D1. YZ mediates radical transfer between the primary chlorophyll donor, P680+, and the metal cluster, at which oxygen is generated from water. This metal cluster or oxygen-evolving complex (OEC) accumulates four oxidizing equivalents, with YZ functioning as the relay on each event. Photosystem II also contains another redox-active tyrosine, YD, which is tyrosine 160 of the subunit called D2. It differs from YZ in that it is not required for oxygen evolution, has a lower potential, and forms a relatively stable radical. As shown in the X-ray structure of Umena et al. (Fig. 1)6, each of these redox-active tyrosines is predicted to hydrogen bond to a histidine. The placement of bound water molecules and proximity to the Mn4CaO5 cluster distinguish YD and
b 4$
c
4% )H
