developing multi-electron catalytic sites in bio-inspired artificial photosynthetic systems for
water oxidation and carbon dioxide reduction.
Controlled Assembly of Ordered Structures. The cofactors that carry out light harvesting and
the primary charge separation in photosynthetic proteins are assembled at specific orientations
and distances to provide optimized function. Moreover, the spatial relationship between the light-
harvesting and reaction-center proteins is optimized for their mutual functioning. Knowledge of
the ways in which these proteins assemble to give specific functional structures remains at an
early stage of development. It is important to understand these processes in detail in order to
apply them to the construction of systems that are hybrids of the natural system with modified
redox components, and so that they can serve as a blueprint for self-assembly of bio-inspired
artificial systems to minimize the synthetic effort required to produce the latter systems and at
the same time provide enhanced functionality.
Compartmentalization of Incompatible Products. The formation of solar fuels requires
reactions that produce both strongly oxidizing and strongly reducing intermediates. For example,
the Photosystem II reaction center, along with the 4-Mn oxygen-evolving complex, generates
redox potentials that are at the limit of what biomolecules can tolerate. Yet the protein provides
an environment in the vicinity of these reactive intermediates that allows a useful number of
catalyst turnovers to occur before accumulated damage results in the protein being replaced. At
this point, very little is known about which protein environments will tolerate a particular
reactive intermediate. Fundamental studies of active site design are necessary to be able to tailor
specialized protective molecular compartments for all reactive intermediates to carry out their
catalytic functions without being destroyed by reacting with their surroundings. This is a critical
feature of catalyst design for both water oxidation and carbon dioxide reduction.
Structural Dynamics. Numerous remarkable advances are being made in the development of
techniques that hold promise for achieving fundamental breakthroughs in imaging the atomic
motions that control light-initiated reactions. These include emerging diffraction and
spectroscopy techniques that exploit pulsed X-ray, neutron, and electron sources to resolve
structural dynamics in a full range of crystalline, amorphous solid phase, and liquid phase
materials. Paradigm shifts that occur with dynamic structural resolution are illustrated by a broad
range of pioneering time-resolved X-ray diffraction and spectroscopy studies that are emerging
for imaging structural dynamics linked to photochemistry. For example, recent 100-ps time-
resolved crystallographic studies of myoglobin have revealed the atomic reorganization events
coupled to porphyrin-bound CO photolysis and identified the unexpected appearance of the CO
across the porphyrin plane (see Figure 40). Equally important are advances in the application of
time-resolved X-ray spectroscopies and coherent and incoherent scattering in non-crystalline
materials. New pulsed X-ray, neutron, and electron sources are providing opportunities to extend
pump-probe X-ray techniques to the picosecond and femtosecond time-domains. Extrapolation
of these techniques to include in-situ resolution of structural dynamics coupled to solar-fuels
production in the non-crystalline media most relevant to solar-energy conversion offer entirely
new opportunities for breakthroughs in resolving the structural basis for energy-conserving
function in both natural and artificial photosynthesis.