Evolution of Photosynthetic NDH-1: Structure and Physiological Function

Abstract

Chloroplast and cyanobacterial NADH dehydrogenase-like complex (photosynthetic NDH-1) is structurally related to the multi-subunit-type NADH dehydrogenase present in bacteria and mitochondria (respiratory NDH-1). They both have a common ancestor, namely the group 4 membrane-bound hydrogenases, including energy-converting hydrogenase (Ech). During its evolution, respiratory NDH-1 (complex 1) acquired the electron input N module that functions in NADH oxidation. Homologs of the N module have not been identified in photosynthetic NDH-1. The electron donor system for photosynthetic NDH-1 has apparently remained similar to that in the common ancestor and accepts electrons directly from ferredoxin (Fd). Indeed, the discovery of the NdhS protein required for high-affinity binding of Fd to NDH-1 in chloroplasts and cyanobacteria supports the idea that photosynthetic NDH-1 accepts electrons from Fd. Through modification of its subunit composition NDH-1 in cyanobacteria is involved in divergent functions, including the concentration of CO2 by NDH-1MS complexes. Nonetheless, chloroplast NDH-1 originated from cyanobacterial NDH-1L that in the light mediates cyclic electron transport around photosystem I (PSI) and in darkness regulates respiratory electron transport. Consistent with this, chloroplast NDH-1 also mediates PSI cyclic electron transport as well as chlororespiratory reduction of the plastoquinone pool in order to maintain redox homeostasis in chloroplasts. During the evolution of land plants, the number of subunits of chloroplast NDH-1 increased and it became associated with PSI to form a supercomplex in flowering plants, the process which is necessary to stabilize NDH-1. Despite conservation of the core skeleton forming the L-shape, photosynthetic NDH-1 is likely to have undergone evolution distinct from that of respiratory NDH-1. Consequently, photosynthetic NDH-1 has gained different physiological functions and operates, at least partially, by molecular mechanisms different from those of respiratory NDH-1.