Friday, September 15, 2017

Origin of water oxidation at the divergence of Type I and Type II reaction centres

Introduction
My friends, the way we think about the evolution of photosynthesis is about to change irreversibly.
I want to share with you some awesome stuff regarding the recent structure of the homodimeric Type I reaction centre by Gisriel et al. (2017) and what I think it all means for the origin of oxygenic photosynthesis. Huge thanks to all the authors. I know it must have been an unbelievable effort.
I have had a chance now to play with the structure a bit. What great pleasure! The structure is amazing and I have seen something that intrigues me enormously. Please, keep reading.
This is the link to the paper describing the structure:
This is a link to the pdb files:
We need first a bit of background though:
In a recent letter to the editor of the Journal of Molecular Evolution I argued that the peculiar structural characteristics of Photosystem II are better explained if water oxidation originated at the divergence of Type I and Type II reaction centres (Cardona, 2017).
What are these peculiar characteristics?
I find quite peculiar that Photosystem II is made of a core, which originated form a Type II reaction centre (D1 and D2) and an antenna, which originated from a Type I reaction centre (CP43 and CP47).
Even more peculiar still is the fact that the CP43 subunit offers a direct ligand to the Mn4CaO5 cluster.
Another peculiar trait about Photosystem II is that D1 and D2 coordinate each a peripheral chlorophyll, ChlZ-D1 and ChlZ-D2. These peripheral chlorophylls and their binding sites are also conserved in Type I reaction centres, but are not found in anoxygenic Type II reaction centres. This means that the most ancestral reaction centre, before the divergence of Type I and Type II, had these peripheral pigments.
The implication of these peculiarities is that an interaction of ancestral Type I and Type II reaction centres is required for the origin of the Mn4CaO5 cluster. A second implication is that this interaction is continuous since the origin of both types of reaction centres, and therefore since very early after the emergence of photosynthesis and the first reaction centres.
So, given the fact that Photosystem II and Photosystem I 'working in series' is the hallmark of oxygenic photosynthesis. And add to this the fact that Photosystem II is a chimera of Type I and Type II reaction centres… it does not take a huge leap forward to think that the initial divergence of both types of reaction centres is actually linked to the origin of water oxidation chemistry.
Think about this for a moment.
This would actually mean that the earliest stages in the evolution of photosynthesis are related to the origin of water oxidation chemistry. In other words, this would mean that oxygenic photosynthesis traces back to the very early stages in the evolution of photochemical reaction centres (Cardona, 2017).
It sounds crazy, right?
Photosystem II and the homodimeric Type I reaction centre
So, what about the homodimeric Type I reaction centre? What about it?
AMAZINGLY, the structure of the homodimeric Type I reaction centre has a Ca-binding site with a number of intriguing parallels to the Mn4CaO5 cluster of Photosystem II:
1. It is positioned exactly where the redox Tyr-His pair is found in D1 and D2 (See Figures 1 and 2).
2. It is connected to the C-terminus by L605 and V608. V608 is the last amino acid in the sequence. In D1 of Photosystem II, the Mn4CaO5 cluster is coordinated by D342 and A344. A344 is the last amino acid of the processed D1 and it ligates not only Mn, but also the Ca!!!!!!!!!
3. It has a connection to the antenna domain, via N263, which is within the 5th and 6th helices. N263 connects to the Ca via two water molecules. In PSII, the CP43 antenna residue E354 offers a ligand to two Mn atoms and it is in the loop connecting the 5th and 6th helices of the antenna! A totally homologous site is also found in D2 and CP47, but phenylalanine residues are found instead of ligands.
4. At the overlapping position where TyrZ/TyrD is, there is a coordinating aspartate.

Figure 1: Panel A shows the Ca-binding site from the reaction centre of H. modesticaldum. In grey I show the connections from the core domain, and in orange the connections from the antenna domain. Panel B shows a schematized version of the Ca-binding site and in italics I have highlighted the parallels with the Mn4CaO5 cluster. In Panel C I show PSII for comparison; and in Panel D I overlap D1 (orange) and PshA (grey). The yellow atom is the Ca of the H. modesticaldum reaction centre.
Figure 2: It shows a comparison of PSII and the homodimeric reaction centre. No doubt that the Ca-binding site and the Mn4CaO5 cluster occupy homologous positions.
Implications for the evolution of water oxidation and the origin of photosynthesis
The main implication is that the most ancestral reaction centre before the divergence of Type I and Type II reaction centres had, at the very least, a Ca-binding site like the one in the structure of H. modesticaldum.
This is strong evidence that the divergence of Type I and Type II reaction centres was due to the development of the structural and energetic requirements to support water oxidation chemistry and the emergence of the oxygen-evolving complex.
This explains why the Mn4CaO5 cluster has a Ca atom! It was there to begin with.
This explains why the Mn4CaO5 cluster has a ligand from the C-terminus. It was there to begin with!
This explains why the Mn4CaO5 cluster has a ligand from the antenna. Guess what? It was there to begin with!
This explains why the site is also mirrored in D2 and CP47, because it all started symmetrically on both sides, as suggested by Rutherford and Faller (2003).
In other words, this implies that the connection from the C-terminus and the antenna domain to the cluster site has been continuous since the emergence of the first reaction centres. Just as I mentioned in my letter!
This also implies that the emergence of water oxidation can be traced to the earliest events in the evolution of photosynthesis. It implies that water oxidation likely predates the diversification of most groups of phototrophs, including Cyanobacteria!
This implies that Cyanobacteria are the only bacteria to have retained water oxidation chemistry, but a greater diversity of oxygenic phototrophs must have predated them.
This is also in perfect agreement with the conclusions of my molecular clock analysis that suggests water oxidation started long before the most recent common ancestor of Cyanobacteria:
This implies that the anoxygenic Type II reaction centres likely evolved from a water-oxidizing Type II reaction centre before the gene duplication event that led to D1 and D2.
I had mentioned earlier that the ancestral Type II reaction centre (before D1, D2 , L, and M) already had some of the components that were needed to evolve the water-oxidizing complex (Cardona, 2015, 2016; Cardona et al., 2015). This validate those observations too.
In the near future, I hope to write something more substantial about this. Put all these ideas together in a nice review: go a bit deeper. In the meantime, it would be nice to discuss what you all think of this madness!
Don't hesitate to leave comments, especially if you strongly disagree and think this is all bonkers.
References
Cardona, T. (2015). A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res, 126(1), 111-134. doi:10.1007/s11120-014-0065-x
Cardona, T. (2016). Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution? Frontiers in Plant Science, 7, 257. doi:10.3389/fpls.2016.00257
Cardona, T. (2017). Photosystem II is a chimera of reaction centers. Journal of Molecular Evolution, 84(2-3), 149-151. doi:10.1007/s00239-017-9784-x
Cardona, T., Murray, J. W., & Rutherford, A. W. (2015). Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol Biol Evol, 32(5), 1310-1328. doi:10.1093/molbev/msv024
Gisriel, C., Sarrou, I., Ferlez, B., Golbeck, J. H., Redding, K. E., & Fromme, R. (2017). Structure of a symmetric photosynthetic reaction center-photosystem. Science, 357(6355), 1021-1025. doi:10.1126/science.aan5611
Rutherford, A. W., & Faller, P. (2003). Photosystem ii: Evolutionary perspectives. Philos Trans R Soc Lond B Biol Sci, 358(1429), 245-253. doi:10.1098/rstb.2002.1186