Article Early Archean origin of Photosystem II
As you may know by now (if you follow my posts or work), the core of Photosystem II is not just made of D1 and D2, but these also have an intimate relationship with the antenna proteins CP43 and CP47. Why is it intimate? Because the CP43 binds the Mn4CaO5 cluster together with D1.
CP43-E354 coordinates two Mn atoms, and CP43-R357 offers a hydrogen bond to one of the Mn-bridging oxygen atoms and it is within 4 Å from the calcium in the cluster.
We have seen now that D2 does not bind a cluster but instead a number of phenylalanine residues seem to replace the ligands and block access to Mn and water. What is remarkable is that CP47 also reaches within D2, as if to provide ligands to a long-gone cluster, but instead it inserts a few phenylalanine residues: one of them within less than 4 Å of the redox tyrosine, YD. Have a look at Figure 7H in the paper.
How? Why? What does this mean? Does it mean that in the homodimeric Photosystem II, before the D1/D2 duplication, the water-oxidising cluster was also coordinated by the antenna domain? Like CP43 does today?
When the crystal structure of the homodimeric Type I reaction centre of heliobacteria was released in 2017, I found a Ca2+ bound to the place where the Mn4CaO5 cluster would be, and these Ca2+-binding sites had a number of structural similarities with the water-oxidising cluster that I thought could not possibly be just coincidence. In particularly, the fact that the putative Ca2+-binding site interacted with the antenna domain in a manner similar to Photosostem II.
I discussed this in an early and hasty version of a manuscript that I should be submitting for publication soon. Have a look:
Working Paper Origin of water oxidation at the divergence of Type I and Ty...
Funnily enough, Prof. Bob Blankenship said in a news article that he didn't believe it. Well, he should believed it, because I'm right! :D haha
https://www.quantamagazine.org/simple-bacteria-offer-clues-to-the-origins-of-photosynthesis-20171017/
I jest.
Anyways, I have now taken a closer look at the antenna's extrinsic domains. And I found something AMAZING.
Have a look at the attached figure with the structural comparisons.
A, B, and C, are the antenna of heliobacteria, CP43, and CP47 respectively. In four different views. In grey you see the transmembrane helices and in colours the extrinsic domain between the 5th and 6th helices. In panel D you can see a schematic view.
I have split the extrinsic domain of CP43 into three bits: EF2, EF3, and EF1.
EF1 is retained in all Type I reaction centres (except PsaA and PsaB) and in CP43 and CP47.
EF3 binds the manganese cluster in CP43. This EF3 region is also found in CP47, but it is at a different location! A change of place occurred!
There is sequence identity in all of the matching domains once they are compared to each other.
Have a look at the attached alignment comparing only the EF3. Sequence identity is unambiguous.
The green arrows indicate the positions where EF3/EF4 are “inserted” in both subunits.
The two residues at homologous positions in the CP47-EF3 region bind a calcium! Yeah, that is right! They bind a calcium!
CP43-E354 is CP47-E435, and CP43-R357 is CP47-N438 as shown in the figure. The Ca2+ is not found in the CP47 of photosynthetic eukaryotes (I did not see it in the structure of the red algae PSII). Except perhaps for the PSII of Cyanophora paradoxa and relatives: early-branching algae.
In CP47, EF1 which in heliobacteria binds the Ca2+, interacts with the CP47-N438 via K332.
The phenylalanine residues that in CP47 insert themselves into D2, are found in the region marked as EF4, which does not exists in CP43.
The level of sequence identity between CP43 and CP47 is about 20%. But this falls to virtually 0% in the extrinsic domain if these are compared in their current order. If you remove EF4, and align the homologous bits together, the sequence identity is back to 20%! Unbelievable.
You might think that 20% overall sequence identity is too low, but the level of sequence identity between the alpha and beta subunits of ATP synthase is also 20%. Just to give you context.
You might think that the CP43 and CP47 have evolved very fast… the opposite is true. Currently after D1 and D2, the second slowest evolving reaction centre subunits are the CP43 and CP47, evolving even slower than ATP synthase today (unpublished data).
All in all it means that EF2, EF3, and EF1 were already present at the moment of duplication!
Given that EF4 only exists in CP47, we can then argue that this was not present before duplication, and therefore the phenylalanine residues that today get inserted into D2 and interact with YD could not have been in the homodimer. So the D2 and CP47 phenylalanine patch could not have been the ancestral state, as it is of course obvious from everything we discussed in the Geobiology paper and what had been described by Bill Rutherford and Wolfgang Nitschke in the 90s (see references in the paper).
Given that EF3 is found in both CP43 and CP47, and that CP43-E354 is conserved as CP47-E435, and similar for position CP43-357 (CP47-438), and given that they still bind something (manganese/calcium), we can then argue that these residues were also available for metal-binding before duplication.
It is consistent with a homodimer photosystem, with clusters on both sides, and with ligands from the antenna. It also strengthens the notion that the Ca2+-binding site in the homodimeric Type I reaction centre is a real thing, and that the structural divergence of Type I and Type II reaction centres is indeed linked to the evolution of the Mn4CaO5 cluster and water oxidation to oxygen.
What this means you can read here:
Article Photosystem II is a Chimera of Reaction Centers
And here:
Preprint Thinking Twice about the Evolution of Photosynthesis
I think that originally manganese and water oxidation started with the help of a small domain similar to that in heliobacteria. A metal-binding site exposed to the media and soluble ions. Once manganese oxidation and an early version of water oxidation got started, the extrinsic domain in the ancestral protein to CP43 and CP47 then increased in complexity, evolving EF2 and EF3 in a drive to provide proton and water channels, to shield the cluster, and to provide a site of interaction with extrinsic polypeptides.
Then the swap of position of EF3 and the evolution of EF4 in the ancestral CP47 contributed to heterodimerization and the loss of water oxidation in D2.
This happens immediatly after the divergence of Type I and Type II reaction centres LONG before the most recent common ancestor of Cyanobacteria.
Did you know that at the gene level, the N-terminus of the CP43 gene overlaps with the C-terminus of the D2 gene contributing a few additional amino-acids to the latter? This is a trait shared by most cyanobacteria, including the earliest branching, and explains how D2 lost the ligands to the cluster located at the C-terminus.
Beautiful, just beautiful.
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