So, when did oxygenic photosynthesis originated? Counterintuitively, the answer to this question does not depend so much on when Cyanobacteria originated. Oxygenic photosynthesis and Cyanobacteria are not strictly the same thing. It actually depends on when photosynthesis and the first reaction centres originated for the first time.
The y axis is time. On the right, we see a species tree of bacteria cantered around the diversity of Cyanobacteria. On the left side, we see a tree of reaction centre proteins.
Let’s focus first on the species tree. It has been recently suggested that the most recent common ancestor (MRCA) of Cyanobacteria capable of oxygenic photosynthesis postdate the Great Oxidation Event (GOE). Shih et al. (2017) suggested that the age of this ancestor is about 2.0 Ga. Similar results had been obtained before in other molecular clock studies, but remained unnoticed, see for example David and Alm (2011). These results have also been reproduced in newer analyses, see for example: (Marin et al. 2017, Betts et al. 2018). There is a real possibility that the MRCA of Cyanobacteria predated the GOE, see for example: (Sanchez-Baracaldo 2015, Sanchez-Baracaldo et al. 2017, Magnabosco et al. 2018). So, let’s not take sides and consider all possibilities.
Cyanobacteria, in the classic sense, are more closely related to the Melainabacteria and Sericytochromatia (Soo et al. 2017). But if we zoom out, the Cyanobacteria/Melainabcateria/Sericytochormatia (CMS) supergroup is thought to be contained within a much larger group that includes Chloroflexi, Actinobacteria, Firmicutes, and the Deinococcus-type. This larger group has been called Terrabacteria by some. I have seen many phylogenomic analysis that puts Cyanobacteria and Chloroflexi as each other’s closest relatives. The estimated time for the Cyanobacteria and Chloroflexi split has been calculated to have occurred about ~3.0 Ga ago by David and Alm (2011) and about ~2.7 Ga ago by Marin et al. (2017). Marin et al. (2017) also timed the MRCA of Terrabacteria at about 2.9 Ga.
Nevertheless, there are phylogenomic trees that put the branch leading to Cyanobacteria very basally in the tree of life of bacteria. See for example: (Hug et al. 2016, Yokono et al. 2018). Also, see the recent tree by Betts et al. (2018). This does not necessarily imply that the MRCA of Cyanobacteria is deeply branching with respect to other bacteria. However, I think overall, the “Terrabacteria” grouping has been reported more often than a basal CMS supergroup for example. Keep this in mind.
Now let’s have a look at the evolution of reaction centres.
Cyanobacteria are characterised by having Photosystem II and Photosystem I. PSII has a heterodimeric core made of the homologous subunits D1 and D2. This core is associated with the homologous core antenna proteins CP43 and CP47. PSI has a heterodimeric core made of the homologous subunits PsaA and PsaB.
The level of sequence identity (distance) between D1 and D2 in ALL cyanobacteria is just under 30%. Between CP43 and CP47 is just under 20%, and between PsaA and PsaB is just under 45%. In other words, the phylogenetic distance between D1 and D2, CP43 and CP47, and between PsaA and PsaB is very large.
The thing about Cyanobacteria is that they all inherited “standard” photosystems. That is to say, that the most recent common ancestor of Cyanobacteria already had photosystems with divergent heterodimeric cores. So, the duplication events leading to D1 and D2, CP43 and CP47, and PsaA and PsaB happened before the MRCA of Cyanobacteria (nodes marked red).
I have attempted to gain an understanding of the evolution of reaction centre proteins as a function of time. I have done that by comparing the levels of sequence identity and by applying molecular clocks under a wide range of evolutionary scenarios (Cardona 2016, Cardona 2018, Cardona et al. 2018).
What I have found is that the gene duplication event leading to D1 and D2, marked as D0 in the tree, is likely to have occurred more than 1 billion years before the MRCA of Cyanobacteria!
It sounds crazy, but it is not crazy at all. It is actually rather straight forward. We’re just not used to think this way about the evolution of photosynthesis. Don’t panic!
In this particular example, the span of time between the D0 duplication event and the MRCA of Cyanobacteria is called ΔT, see the figure.
The large ΔT is due to two facts of life that are pretty unambiguous. 1) The phylogenetic distance between D1 and D2 is VERY LARGE. 2) The rates of evolution of D1 and D2 are VERY SLOW. Therefore, it takes a very long time to span the distance between the D0 duplication event and the MRCA of Cyanobacteria. This is also true for the CP43/CP47 and the PsaA/PsaB duplications.
The rates of evolution of D1 and D2 are very slow, but these rates are not unusual in any way. The rates are just like those in any other highly conserved protein of bioenergetics involved in complex functions. Absolutely nothing peculiar about that. Have a look at Table 3 in Cardona et al. (2018), we have studied the rates of evolution of D1 and D2 in great detail and compared them to those of other proteins.
What is key however, is that the ancestral protein to D1 and D2, D0, likely made a photosystem that was capable of oxidizing water to oxygen or was well on its way towards the origin of water oxidation chemistry. Given the shared conserved traits between D1 and D2 we have a pretty solid idea of what D0 photosystem was capable of doing… and a photosystem made of D0 was not like other anoxygenic Type II reaction centres. That is for sure.
So the roots of oxygenic photosynthesis go deep. I find this conclusion inescapable.
I also found that the rate of evolution of L and M is about 5 times greater than D1 and D2. It appears as if D1 and D2 are actually the slowest evolving reaction centre proteins of all. This means that PSII is the most likely reaction centre to have retained ancestral traits. Counterintuitively as it seems, it is rather evident when you compare the structures of the photosystems… starting from the fact that like Type I reaction centres PSII has retained core antenna proteins and the core peripheral chlorophylls of D1 and D2. What is more, the position of the redox tyrosine residues is located at the ancestral entry point of electrons, as it is the case in homodimeric Type I reaction centres.
I have tried to time the duplication leading to PsaA and PsaB as well (Cardona 2018), which is widely accepted to have occurred after the origin of oxygenic photosynthesis (Ben-Shem et al. 2004, Hohmann-Marriott and Blankenship 2008, Rutherford et al. 2012). It turns out that PsaA and PsaB are also evolving quite slowly, only slightly faster than D1 and D2, in such a way that the PsaA and PsaB duplication likely occurred long before the MRCA of Cyanobacteria too. It is expected that the duplication leading to CP43 and CP47 occurred simultaneously with the duplication of D1 and D2, as they make part of the same complex. The distance between CP43 and CP47 and their rates of evolution agrees with this.
The position of CP43 and CP47 in the tree of reaction centres is not well defined yet. That is why I have put the branch with dashes. That is the position that I think is better supported and has more explanatory power… but other scenarios are possible, all with interesting repercussions. I am currently working on a paper about this.
These three duplications that are unique to oxygenic photosynthesis are more likely to have occurred closer to the origin of reaction centre proteins than closer to the GOE, or after the GOE. Strong arguments supporting the premise that these duplications were driven by the optimisation of water oxidation and the evolution of photoprotective mechanisms to avoid the production of reactive oxygen species can be made. Such arguments can be applied to the initial divergence of anoxygenic and oxygenic specific reaction centre proteins (blue nodes, question marks), see for example (Orf et al. 2018). No matter how you look at it, water oxidation to oxygen likely started well before 3.0 Ga (blue wavy line), which is indeed supported by some geochemical evidence (Planavsky et al. 2014, Satkoski et al. 2015, Havig et al. 2017, Wang et al. 2018).
So how old are these duplications and initial divergences? As you can see in the plot, this depends on how old photosynthesis is. The older reaction centres are, the older the origin of water oxidation chemistry. If we assume that Cyanobacteria is much older than the GOE, then that would make the rates of evolution of reaction centre proteins even slower, which then would push the initial duplications specific to oxygenic photosynthesis (red nodes) even closer to the origin of reaction centres. This is a consequence of the two facts mentioned above, long distance and slow rates.
The origin of oxygenic photosynthesis started in an ancestor of Cyanobacteria… but this ancestor could have been the ancestor of a much greater diversity that could include other Terrabacteria, if that affiliation holds true. Betts et al. (2018) suggested that the MRCA of bacteria is only about 3.4 Ga old. David and Alm (2011) also suggested that the expansion of diversity in bacteria started about 3.4 Ga ago, peaking about 3.2 Ga ago.
I understand that the evidence for photosynthesis at 3.5 Ga (traditionally considered to be anoxygenic) is pretty strong. As far as I understand, the possibility that photosynthesis originated prior to 3.8 Ga cannot be ruled out yet (Rosing 1999, Rosing and Frei 2004, Czaja et al. 2013, Nisbet and Fowler 2014, Butterfield 2015).
Therefore, connect the dots.
If you have questions don’t hesitate to leave a comment.
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