What if light was important for the origin and early evolution of life?

I have become very interested in the idea that photosynthesis and photosynthetic water oxidation was important for the origin and early evolution of life. Call me crazy, but I have reasons!

In this brief post, I will try to present the reasons why I suspect that the emergence of photosynthesis may predate the last universal common ancestor (LUCA).

I have not always thought this way. I have been led to think this way guided by the results of my research. I think the evolution of photosynthetic reaction centres strongly suggests that light was involved in the early evolution of life.

But how?

Please, bear with me.

The reader should know that I am not an expert on Origin of Life research, and I am only superficially familiar with a couple of the different scenarios. I know for example that today the idea that life arose in hydrothermal vents is very popular, although I also know that it is not the only competing hypothesis. In a couple of years, I might be an expert (I am studying hard).

I also know that quite some time ago, it was speculated and considered that the origin of life was somehow photosynthetic, even oxygenic.

For example, Sam Granick wrote in his famous 1957 paper: “It seems more reasonable to consider that the functions of oxidation and photosynthesis were so fundamental that they were part of the first beginnings of protoplasm that arose from inorganic origins.” Then he went on to say: “I propose, as speculation, that the earliest unit around which any living entity arose was an energy-conversion unit. This unit of mineral origin would contain an organization of atoms that would serve as a photocatalyst, at first perhaps in the decomposition of water by UV radiation.”

Today things have changed and scientist do not think this way anymore. Why is that? It is due to a number of reasonable, but unproven assumptions:

1) Photosynthesis has only been discovered in the domain Bacteria, therefore it appears reasonable that the origin of photosynthesis likely occurred after the divergence of Archaea and Bacteria.

2) Oxygenic photosynthesis evolved in Cyanobacteria, so it appears reasonable that the origin of water oxidation is a late invention relative to the origin of life.

In reality, it is a bit more complicated than that as I have recently discussed. This is mainly because the origin of photosynthesis cannot be determined based on a species tree alone. What I mean is that a gene tree and a species tree do not always correspond. So, to understand at what point in the history of life photosynthesis arose we must understand how and when photosynthetic reaction centres and the chlorophyll synthesis pathway arose.

OK, so what is the evidence that suggests photosynthesis is a pre-LUCA innovation?

Allow me to recapitulate several aspects regarding the evolution of photosynthesis.

Firstly, I have concluded that the divergence of Type I and Type II reaction centres predates the divergence of the major groups of bacteria. This is true regardless of the specific evolutionary processes that led to the current distribution of photosynthesis across the tree of life. In other words, the earliest events in the origin of photosynthesis predate the evolution of most groups of bacteria that we know of, including all phototrophs.

There are several reasons why this can be concluded with a good level of confidence. I cannot discuss them here in huge detail because it is not the point of this post, but if you want to know more please see this, this, or just message me for more details. The most important reason, however, is because both Type I and Type II reaction centres make monophyletic clades. Therefore, before we have the Type II reaction centre of purple bacteria or the homodimeric Type I reaction centre of the green sulfur bacteria, we first need to have the processes that led to the ancestor of all Type I reaction centres and the ancestor of all Type II reaction centres.

From this it can also be concluded that at the point in time of the most recent common ancestor of all phototrophs, whatever this was, Type I and Type II reaction centres had already appeared.

Secondly, I have shown that to explain the structural characteristics of Photosystem II, including the coordination sphere of the Mn₄CaO₅ cluster (the oxygen evolving complex), water oxidation must have appeared before, at, or immediately after the divergence of Type I and Type II reaction centres.

Putting these two points together, we then get that water oxidation chemistry originated before the diversification of most groups of bacteria, including Cyanobacteria.

Thirdly, I attempted to understand the evolution of Photosystem II as a function of time. What I discovered is that the roots of Photosystem II, as determined by the gene duplication leading to the heterodimerisation of the photochemical core (D1 and D2), trace back to long before the most recent common ancestor of Cyanobacteria. This boils down to the fact that the rates of evolution of Photosystem II are tremendously slow. It is a bit more complicated than that, but this should suffice for the moment.

At this point we have traced photosynthetic water oxidation to an early stage in the evolution of the domain Bacteria.

But how we go from there to before the LUCA?

Warning! I am not trying here to explain the origin of life. I am no trying to come up with a reasonable evolutionary scenario. I am only following the evidence at hand, which is directly derived from the study of the molecular evolution of the reaction centres.

About two years ago, I was at a local meeting at Imperial. I presented my research on the evolution of Photosystem II and a well-known Nobel Prize winner mentioned that the evolution of ATP synthase seemed to share some similarities with Photosystem II.

Basically, the photochemical core of Photosystem II is made of two homologous subunits, D1 and D2. Catalysis occurs in D1. The catalytic core of ATP synthase is made of two homologous subunits, the alpha and beta subunits: they make the hexameric head. The beta subunit has the catalytic active site.

To provide further support that Photosytem II and water oxidation is as old as I suggested in the Geobiology paper, I thought that it would be a good idea to compare it to the evolution of other enzymes. I wanted to compare the D1/D2 and CP43/CP47 duplication events with one duplication that is known to be very ancient and with a duplication that is known to be very recent.

ATP synthase is a perfect point of reference for the very ancient duplication, not only because of those similarities with Photosystem II, but also because we know that the duplication leading to alpha and beta predate the LUCA.

Therefore, if Photosytem II emerged long after the LUCA: then, given the slow and very predictable rates of evolution of these complexes, major differences in evolutionary patters should be absolutely clear.

What I found is that Photosystem II evolves at a slower rate than ATP synthase.

I am talking here of some of the slowest rates of evolution in all biology.

ATP synthase evolves so slowly that even though the duplication leading to alpha and beta occurred before the LUCA, they still retain about 20% sequence identity and they are still structurally very similar. That is slow enough so that after billions of years of evolution strong sequence and structural identity is retained. Because the duplication is so old, then it makes sense that after billions of years the level of sequence identity between alpha and beta is relatively low.

Well, Photosytem II evolves slower than ATP synthase! And the core subunits, D1 and D2, show 29% sequence identity. The antenna of Photosytem II, CP43 and CP47, which also originated from a gene duplication event have about the same level of sequence identity as alpha and beta, 18%. And guess what, the rate of evolution of CP43 and CP47 is only slightly slower than the rate of alpha and beta.

From this reference.

Under similar conditions D1 and D2 are evolving at about 0.12 ± 0.04 amino acid changes per site per billion years (Cardona et al. 2019). CP43 and CP47 at about 0.19 ± 0.04 amino acid changes per site per billion years (unpublished) and alpha and beta at about 0.28 ± 0.06 amino acid changes per site per billion years (unpublished).

This means that there is no differences in the evolutionary patterns of the ATP synthase catalytic unit when compared to the core of Photosystem II! No matter how I model their evolution, I will not be able to place the origin of Photosystem II after the origin of ATP synthase.

The rate of evolution is strongly related to the complexity of the system. A case could be made to argue that all reaction centres show greater complexity than ATP synthase.

Therefore, the earliest stages of Photosystem II evolution could be coincidental or might slightly predate those leading to V-/F-type ATP synthases. If this is the case, then water oxidation and photosynthesis predates the LUCA.

Again, I want the reader to understand that I am not trying to come up with an origin of life scenario based on a collection of reasonable assumptions.

This is the path that the evidence has pointed towards…

Imagine the ribosome. Kind of in between the origin of information processing and protein synthesis. A complex molecular machine made of protein and RNA.

Imagine now reaction centres. Forget everything you know about reaction centres and look at them with fresh eyes. A bag of cofactors and proteins unlike anything else in biology. What if they emerged at the interface between the pre-biotic synthesis of porphyrin-derived compounds and the very first proteins involved in photochemical energy conversion and electron transfer?

I find beauty and harmony in this view.