pf-pt

Plenary Talk

Evolution of the Function of Photosynthetic Reaction Centers: Insights from the Heliobacterial Reaction Center

Gregory Orf, William Johnson, Christopher J. Gisriel, Raimund Fromme, and Kevin E. Redding*

School of Molecular Sciences, Arizona State University, Tempe, Arizona 85280.

*Email: Kevin.Redding@asu.edu

The proliferation of phototrophy – the use of light as a biological energy source – within early prokaryotes represented a significant step forward in metabolic evolution. All available evidence supports the hypothesis that the photosynthetic reaction center – the pigment-protein complex in which electromagnetic energy is converted to chemical energy usable by an organism – arose once in the history of this planet over 3 billion years ago, and its basic architecture has been diversified into the distinct versions that now exist. Using our recent 2.2-Å X-ray crystal structure of the homodimeric photosynthetic reaction center (RC) from Heliobacteria, we have compared all known RCs with available structural data. This has allowed us to generate hypotheses about structural and functional aspects of the common ancestors of extant RC and to expand upon existing evolutionary schemes. In the evolutionary trajectory I will discuss, the ancestral RC predating the division between Type I and Type II RCs was homodimeric, loosely bound two quinones, and performed a slow, light-driven disproportionation reaction to reduce quinone to quinol. The changes leading to the diversification into Type I and Type II RCs were different responses to the need to accelerate this reaction. The Type I lineage added an FeS cluster to facilitate double reduction of quinone. The Type II lineage heterodimerized and specialized the two cofactor branches, fixing the quinone in one of the sites. Fixation of the quinone sites followed by heterodimerization to allow asymmetric binding of a new subunit containing additional FeS clusters then occurred in an ancestor to Photosystem I as a protective response to rising O2 after the appearance of the water oxidation complex in an ancestor of Photosystem II.

Figure 1. Structure of the heliobacterial reaction center (side view)

Gisriel C, Sarrou I, Ferlez B, Golbeck JH, Redding KE, Fromme R (2017) Structure of a symmetric photosynthetic reaction center-photosystem. Science 357:1021-1025.