Reconstructing the Origin of Oxygenic Photosynthesis: Do Assembly and Photoactivation Recapitulate Evolution?

Abstract

Due to the great abundance of genomes and protein structures that today span a broad diversity of organisms, now more than ever before, it is possible to reconstruct the molecular evolution of protein complexes at an incredible level of detail. Here, I recount the story of oxygenic photosynthesis or how an ancestral reaction center was transformed into a sophisticated photochemical machine capable of water oxidation. First, I review the evolution of all reaction center proteins in order to highlight that Photosystem II and Photosystem I, today only found in the phylum Cyanobacteria, branched out very early in the history of photosynthesis. Therefore, it is very unlikely that they were acquired via horizontal gene transfer from any of the described phyla of anoxygenic phototrophic bacteria. Second, I present a new evolutionary scenario for the origin of the CP43 and CP47 antenna of Photosystem II. I suggest that the antenna proteins originated from the remodeling of an entire Type I reaction center protein and not from the partial gene duplication of a Type I reaction center gene. Third, I highlight how Photosystem II and Photosystem I reaction center proteins interact with small peripheral subunits in remarkably similar patterns and hypothesize that some of this complexity may be traced back to the most ancestral reaction center. Fourth, I outline the sequence of events that led to the origin of the Mn4CaO5 cluster and show that the most ancestral Type II reaction center had some of the basic structural components that would become essential in the coordination of the water-oxidizing complex. Finally, I collect all these ideas, starting at the origin of the first reaction center proteins and ending with the emergence of the water-oxidizing cluster, to hypothesize that the complex and well-organized process of assembly and photoactivation of Photosystem II recapitulate evolutionary transitions in the path to oxygenic photosynthesis.

Early emergence of the FtsH proteases involved in photosystem II repair

“…Similarly, FtsH proteases involved in PSII repair (SynFtsH2/3) branch out before the divergence of Group 1 FtsH in Chloroflexi and Proteobacteria. Cyanobacterial PsaA and PsaB, the core subunits of PSI, also branch out before the divergence of PshA and PscA of anoxygenic homodimeric Type I RC proteins of Heliobacteria, Acidobacteria, and Chlorobi (Cardona 2015(Cardona , 2016b, with heliobacterial PshA branching out before PscA. This is also mirrored in the tree of Group 1 FtsH proteases of phototrophs, with FtsH sequences involved in PSII repair branching out before those present in anoxygenic phototrophs containing Type I RCs.…”

“…However, recent detailed analysis of the phylogeny of RC proteins indicates that HGT of RCs to an ancestral nonphotosynthetic cyanobacterium from anoxygenic phototrophic bacteria is unlikely (Cardona 2016b); furthermore, the evolution of RC proteins shows that the last common ancestor to all phototrophic bacteria had already evolved Type I and Type II RC proteins from an earlier gene duplication event (Sousa et al 2013, Harel et al 2015. In addition, it has been argued that the evolution of the structural complexity of PSII and the origin of the oxygenevolving manganese cluster can only be explained if both types of RC had been evolving in cooperation since the dawn of photosynthesis and that water oxidation might therefore have occurred at a far earlier stage of evolution that previously thought (Cardona 2016b(Cardona , 2017. This translates to the phylogeny of RC subunits in PSII and PSI showing a significant phylogenetic distance to those in anoxygenic phototrophs assuming similar rates of evolution (Cardona 2015.…”

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

“…Therefore, it is possible that these mutational enrichment periods correspond to the adaptation of key oxygen‐sensitive components of Rubisco prior to the GOE (Anbar et al., 2007; Planavsky, Reinhard, et al., 2014). This would further indicate that calibrating the Rubisco tree to the appearance of cyanobacterial fossils or the GOE itself must be undertaken with care, given the possibility that stem group oxygenic photosynthetic organisms could have existed long before the appearance of recognizable Cyanobacteria in the fossil record (Blankenship & Hartman, 1998; Cardona, 2016; Fischer, Hemp, & Johnson, 2016; Johnson et al., 2013). Phenotypic characterization of expressed and purified ancestral forms of Rubisco may provide a biochemical and physiological basis for correlating the specific site mutations between the Anc.…”

Photosystem II is a Chimera of Reaction Centers

“…Figure 1 shows that these are absent in anoxygenic Type II reaction center proteins (L and M) but they have been retained in Photosystem I and anoxygenic Type I reaction centers from heliobacteria and green sulfur bacteria (Cardona 2015). I pointed out before that sequence and structural homology in this region strongly suggest that these peripheral pigments are a trait present in the most ancestral photochemical reaction centers before the divergence of Type I and Type II reaction centers (Cardona 2016). Now, the fact that these pigments have been retained in Photosystem II, as energy connectors between the reaction center (Type II) and the core antenna (Type I), argues definitively that the close interaction between the two type of reaction centers is continuous since the origin of photosynthesis, throughout the early diversification of Type I and Type II reaction centers, and until the origin of the Mn4CaO5 cluster in Photosystem II.…”