Evolution of Photochemical Reaction Centres: More Twists?

Tanai Cardona,A William Rutherford

doi:10.1016/j.tplants.2019.06.016

Abstract

One of the earliest events in the molecular evolution of photosynthesis is the structural and functional specialisation of type I (ferredoxin-reducing) and type II (quinone-reducing) reaction centres. In this opinion article we point out that the homodimeric type I reaction centre of heliobacteria has a calcium-binding site with striking structural similarities to the Mn4CaO5 cluster of photosystem II. These similarities indicate that most of the structural elements required to evolve water oxidation chemistry were present in the earliest reaction centres. We suggest that the divergence of type I and type II reaction centres was made possible by a drastic structural shift linked to a change in redox properties that coincided with or facilitated the origin of photosynthetic water oxidation.

Highlights

A complete scenario for the evolution of oxygenic photosynthesis should first explain how and when water oxidation to oxygen originated at the level of the photochemical reaction centre
In Photosystem II (PSII) the Mn4CaO5 cluster is coordinated by D1 and CP43 (Figure 2) [11]
These two residues are located in an extrinsic protein domain between the 5th and 6th helices of CP43 that reaches into the electron donor-side of D1

Summary

Evolution of Photosystem II

There is no consensus on when and how oxygenic photosynthesis originated. Both the timing and the evolutionary mechanism are disputed. The recent structure of the homodimeric Type I reaction centre [19] from a basal anoxygenic photoheterotrophic firmicute, Heliobacterium modesticaldum, revealed a previously unknown Ca2+-binding site with a number of intriguing parallels to the Mn4CaO5 cluster of PSII (Figure 3). This Ca2+binding site is positioned at the electron donor side of each monomer of the reaction centre, in a location corresponding to that of the redox tyrosine-histidine pair in D1 and D2, in the immediate vicinity of the. The position of PufC (the tetraheme cytochrome of anoxygenic Type II reaction centres, see Figure 1) and its evolution as an electron donor, represent a novel adaptation rather than the primitive ancestral state of Type II reaction centres

The divergence of Type I and Type II reaction centres

Increasing the potential of the acceptor side

Final remarks

Methods