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?
