Solar-to-Chemical Conversion

Figure 3.12Two selected scenarios for the nature of the S 4state and O—O bond formation from the computational literature: (a) formation of a Mn1(IV)‐oxyl group in the S 4state is followed by odd‐electron radical oxyl–oxo coupling [285], and (b) formation of a five‐coordinate high‐spin Mn4(V)‐oxo is followed by intramolecular nucleophilic coupling with concerted water binding [289]. Thick lines indicate direction of Jahn–Teller axes of Mn(III) ions.

It should be clear from the above that despite enormous strides, several aspects of the biological system, including its exact atomistic structure and crucial mechanistic details, remain incompletely understood for the later steps of the catalytic cycle. In the effort to better understand the natural water oxidation catalyst, a major target has been the synthesis of molecular mimics that reproduce structural and electronic properties of the OEC [302]. Following a long history in the development of oligonuclear manganese model complexes [303–305], the past decade has witnessed seminal achievements with the synthesis of manganese–calcium clusters that closely mimic the stoichiometry, metal oxidation states, and bonding topology of the OEC [306–318]. Landmark reports by the groups of Agapie [307] and Christou [308] established access to Mn(IV) 3CaO 4cubanes, whose magnetic properties (ferromagnetic coupling to a total S = 9/2 state) mirror those of the cuboidal subunit of the OEC in specific states [198]. Zhang et al. [314] subsequently achieved the synthesis of a complex with a Mn 4CaO 4core that reproduces the arrangement of metal ions of the OEC and has oxidation states equivalent to the S 1state of the OEC, Mn(III) 2Mn(IV) 2. Moreover, the complex can be oxidized and produces spectroscopic signatures similar to those of the natural system [237, 314]. Extensions of this work include variants of the original complex with exchangeable solvent molecules [316].

Molecular biomimetic complexes are indispensable for elucidating structure–property correlations of relevance to the OEC, and they are a valuable source of insight into how specific geometric or electronic features of a polynuclear manganese cluster affect its overall properties and function [319–323]. At the same time, it should be acknowledged that structural mimics of the OEC have not been linked so far to appreciable water oxidizing activity. Water oxidation has been known for heterogeneous manganese oxides [324–328], but as far as molecular systems are concerned, manganese complexes reported to catalyze oxygen evolution are typically not direct mimics of the OEC, while their performance lags far behind noble metal molecular or solid‐state catalysts [324–328]. There is undoubtedly vast unexplored potential for the development of biomimetic manganese‐based molecular water oxidation catalysts. However, our current understanding of the biological system strongly indicates that its catalytic ability is not simply encoded in the structure of the inorganic cluster of the OEC, but depends critically on the protein matrix that both fine‐tunes the properties of the cluster and performs crucial functions in terms of managing proton‐coupled electron transfer and regulating the flow of substrate and product. Therefore, it is conceivable that any small‐molecule mimic of the OEC, although useful as structural and electronic analog of the biological active site, is destined to fail as a practical water oxidation catalyst because it will not be able to reproduce the functionality that is taken care of by the PS‐II enzyme as a whole. Promising approaches that would be arguably more suitable for large‐scale realization of artificial photosynthesis are discussed in subsequent chapters.

Capture of CO 2and reduction to products such as CO, HCOOC, H 2CO, CH 3OH, or CH 4are a principal target for artificial photosynthesis in the quest for solar fuels, as discussed in detail elsewhere in this book. A strictly biomimetic approach does not seem ideal in this case compared to photocatalytic and (photo)electrochemical reduction of CO 2. However, there are still lessons to be learned from biology, and here we will briefly cover the CO 2fixation process in natural photosynthesis, which is carried out by the enzyme RuBisCO (ribulose‐1,5‐bisphosphate carboxylase/oxygenase) [4]. RuBisCO is considered the most abundant protein on earth [347, 348] and uses CO 2to convert the five‐carbon molecule ribulose‐1,5‐bisphosphate (RuBP) to two three‐carbon 3‐phosphoglycerate (3PGA) molecules, one of which incorporates the CO 2‐derived carbon atom. This carboxylation reaction provides the substrate for subsequent reactions in the Calvin–Benson cycle that phosphorylate and reduce 3PGA using ATP and NADPH to produce glyceraldehyde 3‐phosphate (G3P), the precursor molecule of glucose and other carbohydrates. In most photosynthetic organisms RuBisCO is present as a complex composed of eight copies of large (L) proteins and eight copies of small (S) proteins, L 8S 8[349]. The active form of the enzyme is generated by carbamylation of an active site lysine residue [350] via reaction with CO 2and subsequent binding of Mg 2+at the carbamate. This is the form that binds RuBP, at the Mg 2+ion [351]. The carboxylation reaction is thought to proceed by initial creation of the enediol form of RuBP, which reacts with CO 2and is hydrated before C—C bond cleavage and release of the two 3PGA molecules ( Figure 3.13).

Figure 3.13Reaction mechanism of RuBisCO proposed by Taylor and Andersson.

Source: Taylor and Andersson [351].

RuBisCO evolved at a time when the atmosphere of our planet was much richer in CO 2and did not contain much O 2. The oxygenation of the atmosphere posed a serious challenge for RuBisCO because O 2is a competitive substrate to CO 2. Binding of O 2by RuBisCO leads to an alternative reaction pathway that results in oxygenation of RuBP. This is an unproductive pathway (photorespiration) that leads to creation of 2‐phosphoglycolate (2PGA) and eventual loss of previously fixed CO 2. Although several adaptations at the cellular or metabolic level exist in biology to deal with this problem, evolution has not come up with a “solution” at the molecular level, i.e. with restriction of oxygenase activity by adaptation of the enzyme itself. The inability of RuBisCO to discriminate strongly between CO 2and O 2is considered to be the reason for the utilization of very large quantities of the enzyme by photosynthetic organisms and is viewed as the primary reason for the low overall efficiency of natural photosynthesis [352–355].

Natural photosynthesis can show us how evolution solved the problem of converting solar to chemical energy to serve the biological needs of living organisms. The fundamental components of natural photosynthesis are conceptually the same as in any conceivable practical realization of artificial photosynthesis: light harvesting, charge separation, water oxidation, and CO 2fixation. Many of the specifics of natural photosynthesis serve as blueprints and provide inspiration for the development of synthetic systems that might be conceived as “artificial leaves” [356, 357]. The operating principles of the OEC and its smart protein matrix are preeminent examples in this respect. However, there are other aspects of natural photosynthesis that are not ideal templates to be imitated in technological applications, such as nature's utilization of CO 2to produce biomass. Research in natural photosynthesis and on the multiple questions that remain open, such as the details of water oxidation, will continue in tandem with efforts to develop artificial systems. It is hoped that insights from the former will fertilize the latter, because even if the future of artificial photosynthesis is not strictly biomimetic, it is inevitable that design principles will be shared.