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Hello and welcome. You are listening to a
podcast by the Miller Centre for Evolution at
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the University of Bath. I'm Professor Turi King,
your host, and today I'm talking to Tom Williams,
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Professor of Computational Evolutionary Biology.
Tom uses computational methods to study how
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molecules, genomes of microbes evolve and to
learn about the evolutionary history of life.
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Tom has just been part of a big study trying to
understand the evolution of eukaryotic cells,
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a formative event in the history of life on Earth.
Tom, before we get into your study,
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let's back up a bit. What was life
like on Earth before eukaryotic cells?
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So, from what we know, we think that life started
on Earth pretty soon after the planet's formation.
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So, the Earth is about 4.5 billion years old.
That's when the moon was created, and you get
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the Earth moon system as it is today. And based on
what we can tell within about 300 million years of
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that period, you already had simple cells living
on Earth. So, what we call prokaryotic cells.
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So today, the bacteria and the archaea have
prokaryotic cells. They're relatively small.
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So maybe one micron across. They don't
have a huge amount of internal structure.
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But all of these rather simple cells, at least
structurally, are very biochemically diverse,
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very metabolically diverse.
And so, we think relatively early
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in life's evolution on Earth, within the first,
let's say, 1 to 2 billion years of life's history,
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a lot of the different metabolisms and ways of
life that single celled organisms use today
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would have already existed. So, from things
like methanogenesis through to, you know,
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oxygenic photosynthesis, like cyanobacteria
and plants do today, on the early Earth,
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all of these metabolisms would have been
evolving in a relatively oxygen free environment.
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So, what distinguishes these really simple
prokaryotic cells from eukaryotic cells?
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What's the difference between them?
Yeah, I mean, when you look at life
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as it's organized today, that you've got
the prokaryotes, as I've already mentioned,
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and the eukaryotes. And eukaryotic cells are
typically much larger than prokaryotic cells,
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perhaps 10 to 100 times as big in diameter. In
particular, they're very structurally complex.
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So, they're full of lots of internal compartments.
The eukaryotic cells have got a nucleus which
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contains the genes, which are the blueprint for
the cell. They've got mitochondria, those are
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compartments in the cell that produce energy.
And then in photosynthetic eukaryotes, like
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in plants and algae, you've got compartments like
the chloroplast where photosynthesis happens. And
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there's lots of other subcellular structures too.
So, they're much larger, more complex, and perhaps
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also more structurally dynamic cells. So, they're
capable of lots of different sorts of movement.
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And the other thing, the other aspect of
eukaryotic complexity is that all of the
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most familiar, like multicellular groups
of life that we know. So, animals, plants,
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fungi, seaweeds, slime molds, they're
all made up of eukaryotic cells. So,
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it's not just that individual eukaryotic cells
are bigger and more complex than prokaryotes,
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but also these most familiar forms of life
are all made up of sort of agglomerations
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of large numbers of eukaryotic cells.
I mean, this is obviously a really big
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event in evolution because you go from these
really simple cells to these much bigger,
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much more complex cells that kind of make-up,
as you say, pretty much what we kind of think
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of as life on Earth these days. The plants
and the animals and us, for example. So how
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do we think that happened? That step from those
really simple cells to these more complex cells?
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So, we don't know all the details, and, you
know, the study that we're going to talk
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about is trying to look at one aspect of that.
But I think the sort of fundamental idea here,
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which has been established now for quite
a while, is the idea of endosymbiosis.
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So, the endosymbiotic theory, which is the
idea that the first eukaryotic cells came
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together through symbiosis of simpler prokaryotic
cells. So, one cell coming to live inside another,
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and in that way you get sort of a larger
compartmentalized cell. And, in particular, the
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idea is that there was a host cell which was drawn
from the archaeal domain of life. A member,
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we think of the Asgard archaea, so one group
of archaea, and its genome has its descendants
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today in the nucleus of eukaryotic cells.
And then on the other side, we think its symbiotic
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partner was an alpha proteobacterium. So that's
one particular type of bacterium which evolved to
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become the mitochondria in this energy producing
compartment of the eukaryotic cell. And that's
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a really core aspect of the theory. But beyond
that there's a lot of details that are debated.
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So actually, let's go back for a second,
what's archaea. Because I think people
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know what bacteria is. But the average listener
won't know what archaea is. So, what are archaea?
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So, archaea are another group of prokaryotic
cells. So, under a light microscope they're
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hard to tell apart from bacteria. But actually,
if you look at their DNA or their metabolism,
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they are very distinct from bacteria. And
we actually think that the deepest split
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in the tree of life is between these two major
lineages of prokaryotes, the archaea and bacteria.
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In terms of their cell biology, the way
that they make their cell membrane is a
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little bit different. And they have a number
of kind of unique metabolisms which you don't
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find in bacteria, in particular methanogenesis. So
that's a way of making energy from reacting carbon
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dioxide with hydrogen. So, there's some other
varieties of that as well. And these archaea,
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you know, they're globally very abundant and
they're found in many different environments.
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When they were first discovered, which is
relatively recently. Right, so we're talking about
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the late 1970s by Carl Woese and his colleagues.
The idea was that archaea were restricted to
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extreme environments, so they might be living in
very acidic environments or very hot environments.
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But actually, in recent decades, particularly as
techniques for sequencing genomes directly from
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the environment have been developed, we've
discovered that archaea are actually found
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in many different environments, including
the same sorts of environments we live in.
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There are some living in our microbiome, for
example, in soils, they're very common. So,
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they're abundant, they're globally distributed,
and they're an important part of, I guess,
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life's prokaryotic genetic diversity.
So, you've got these two simple cells coming
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together, one sort of is engulfing the other. But
instead of it being munched and eaten, it actually
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sort of just lives inside this other cell. So,
what are the big questions here? Presumably,
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it's about timing and how that happened and
how these kind of more complex structures
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within eukaryotes arose, I'm guessing?
Yeah. That's right. I mean, there's a
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lot of different questions that people are
investigating in regard to how that symbiosis
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took place and its role in the evolution of
eukaryotic complexity. But I think one of
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the big questions is how complex a cell was the
archaeal host which entered into this symbiosis
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with the mitochondrion. And there's sort of a
continuum of views of which you have two extremes.
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At one extreme, which is called the mitochondria
early view, the two cells which initially
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interacted to form that symbiosis, where both very
simple prokaryotic cells, just like we might see
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among prokaryotes today. And it's actually the
coevolution or the sort of symbiotic integration
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of the two, the way that they were sort of forced
to evolve to live together and to integrate,
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which catalysed the development of all of
these complex features of eukaryotic cells.
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At the other end of the continuum, you have
scenarios in which this symbiosis between
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the archaea and the bacterium was actually
a relatively late stage in the evolution of
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eukaryotic complexity. And the idea there
is that the archaeal host cell might have
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already had some of the kind of cell biological
features that we associate with eukaryotes,
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things like, for example, the cytoskeleton,
maybe even the ability to phagocytosis or to
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sort of eat food, if you think of the way
macrophages or amoeba engulf their prey,
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that sort of way of eating other cells.
And it's a sort of intermediate spectrum
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of hypotheses you could imagine as well.
In which some of those cellular features
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have already evolved, and some came after the
mitochondrial endosymbiosis. And a lot of the
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debate is about the order of the events and
the causative role that each of those traits
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played during the evolution of eukaryotes.
And this is exactly what you've been looking
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at in your paper. So, tell me about
your paper, what have you been doing?
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Yeah. So, what we really tried to do in this
paper is to work out the order in which some of
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these key traits of eukaryotes evolved, relative
to the timing of the mitochondrial acquisition,
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the timing of this endosymbiosis. And the way
that we tried to do that is by linking the
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origin of each of these traits to certain genomic
features, which we could try to date using some
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molecular clock or phylogenetic methods. So, in
particular, we tried to date events known as gene
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duplications during the evolution of eukaryotes.
So, when you're thinking about how new functions
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can evolve in life’s evolution, or you’re
thinking about how complexity can evolve,
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the idea of gene duplication is one of the key
mechanisms. So, the starting point would be a
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single gene in an ancestral organism, which
encodes some particular function. Let's say
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maybe it's encoding one of the polymers that's
involved in making the cytoskeleton. The idea is
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that if you've just got a single gene that's
playing an important role in an organism,
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it doesn't really have a scope to evolve because
it's got to keep playing that important role.
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However, if the gene gets duplicated,
so that you now have two copies,
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and that can happen because of an error during
genome replication, for example, you now have
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a situation where what's possible in sort of
selective or evolutionary terms is different,
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because now one of those two copies could keep
playing the ancestral function that needs to be
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maintained, while the other could evolve a new
function which changes how that cytoskeletal
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filament forms. Or maybe it changes the
compartment in which a gene should be expressed.
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And so, as you look at the origin of eukaryotes,
we can see by doing comparative genomic analyses
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that there are a lot of gene duplications in
functions that are associated with these eukaryote
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specific traits. So, what we tried to do in this
paper then is identify gene duplication events,
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which we could link to the origin of these
traits and then use molecular clock analysis
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to try to date them. And then with those
dates, we've got the sort of timeline for
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when each of the features evolved.
So, talk me through the molecular
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clock analysis. How does that work?
The molecular clock hypothesis,
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the idea of a molecular clock is that the rate
at which genomes change in evolutionary time is
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constant. So, genomes might pick up changes like
the ticking of a clock. That's the original idea,
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and it comes from really sort of conceptually
brilliant work from Pauling and Zuckerkandl.
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And unfortunately, the molecular clock hypothesis
in that very pure form isn't true. Actually,
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organisms evolve at very different rates for
all sorts of different reasons. They might be
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living in different habitats, they could be
experiencing different selective pressures,
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or they might have different DNA replication
machineries that just sort of make mistakes at
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different rates. So actually, the molecular clock
ticks at a different rate in different lineages.
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So that makes trying to determine when things
happened in the past a statistical problem,
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because we can have a statistical model
which tries to learn about what the rates
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of evolution are in different lineages. And
if we have a model like that, we can feed
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in information about these gene duplications
from modern genomes and try to work out when
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they happened at particular times in the past.
And those types of models are called relaxed
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molecular clock models. That's because they don't
assume a single rate of evolution that's sort of
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been constant through time, but they do allow you
to combine genetic information with what we call
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calibrations. So that could be fossil information
that tell us about when ancestors lived in the
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past, to estimate when these features evolved.
And what did you find?
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Well, what we found was that the acquisition
of the mitochondrion appears to have been a
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relatively late event during this process of the
origin of eukaryotes. And the evidence for that,
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the reason that I say that is that some of the
gene duplications in the archaeal host side of
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the eukaryotic family tree, gene duplications
associated with, for example, the development
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of this cytoskeleton, the endomembrane system,
so that means the way that eukaryotes have many
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different internal compartments and can move
materials between compartments, and even some
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aspects of the development of the eukaryotic
nucleus. These gene duplications, we think,
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happened in some cases several hundred million
years before the acquisition of the mitochondrion.
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So, what we think is between a period of about 3
billion years ago and roughly 2 billion years ago,
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there was, in geological terms, a sort
of a gradual, complexification of the
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eukaryotic cell, with the mitochondrion
being relatively late in that process.
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So why is this event where mitochondrion become
kind of acquired into the eukaryotic cell? Why
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is that such a big deal… it’s clearly a very
big deal because people are really interested
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in when it happened. Why is it a big deal?
Well, I think there's sort of quite diverging
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views on that, but for sure it's
one of the key features that defines
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eukaryotes. One thing to say is that almost
all eukaryotes today have got mitochondria.
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There's a really small number that don't. But
it's not that they never had mitochondria,
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rather it's that they've lost them. And that's
because they've moved into environments perhaps
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where they don't need mitochondria anymore.
And so, what the original function of the
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mitochondrion was, there's I think,
several very reasonable ideas.
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One thing to note is that around the time that we
think the symbiosis between the archaea and the
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bacterium which became the mitochondrion happened,
around that time, an event occurred called the
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Great Oxidation Event. So that's a time when the
planet went from being largely anaerobic. So,
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with very little free oxygen for use in
metabolism, to something not quite like today,
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but where levels of free oxygen began to
accumulate, at least to an appreciable level.
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And that had a huge influence on ecosystems
because now organisms could use oxygen in
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their metabolisms and generate energy, often
much quicker than they were able to before.
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So, one possibility is that by acquiring the
mitochondrion this symbiotic lineage was
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able to make use of that oxygen, because we think
the mitochondrion would have had an aerobic,
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so oxygen using metabolism. The archaeal partner
perhaps not, though like a lot of details here,
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it's very hard to be sure about
any of this. So that's one aspect.
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But another really important thing when it comes
to the acquisition of mitochondria, is that it
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potentially would have changed energy availability
for the cell. So, this is again an area where
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people debate. But one really important feature
of the way organisms actually conserve energy
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or generate energy, if you like, is that it's
typically done on the membrane of the cell. So,
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organisms generate a proton gradient, so gradient
of hydrogen ions over the cell membrane. And then
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this gradient is harnessed by protein complexes
called the ATP synthase machinery. Sort of like
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water going through a water wheel if you like,
to generate energy as the protons flow back into
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the cell. In prokaryotes they've got a single
cell membrane, typically the outer membrane,
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and that's the site at which they can
harness energy from these proton gradients.
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But in eukaryotic cells, at least eukaryotes
that have multiple mitochondrial compartments,
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they can actually use much more surface area of
membranes to generate energy. And this shift,
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a kind of a structural or topological shift in
the way that cells could generate energy could
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have been important for early eukaryotes as well.
But not everybody would agree with that idea,
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and there's lots of different opinions there.
But we certainly think that harnessing oxygen
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was something important that mitochondria
brought to the table for eukaryotes.
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So, what’s coming across talking to you is
that not only is this one of the biggest
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events in evolution, and perhaps that's
why it's such a controversial area. So,
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talk me through the controversies.
It is a controversial area and it's a very
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interesting area to work in. I think one of the
things I like most about working on these sorts of
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eukaryote origins questions is that it's a
very conceptually rich area. So, there's a
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lot of different hypotheses, a lot of different
ideas. What I've tried to do is come up with
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some computational ways of testing, some of those
hypotheses. But I think there's disagreements and
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there's debates along several different axes.
Fundamentally, one of the issues is there just
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isn't that much data. So, we're working in a
relatively data poor area of science. Though
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in recent years, environmental genomics,
where we've obtained genome sequences from
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lots and lots of new groups of microbes, have
actually provided lots of new, relevant data.
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But it's definitely an area where there's
huge uncertainties. And so reasonable people
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often disagree about how things proceeded.
It's also an area which has attracted interest
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from people with many different interests and
backgrounds. So, people who are interested in
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molecular evolution like me are often working on
this question. But there's also palaeontologists,
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cell biologists, you know many different groups of
people. And often they suggest hypotheses which,
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in part, directly disagree,
but also to a certain extent,
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are addressing different aspects of the problem
of eukaryogenesis, of the origin of eukaryotes,
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right. So, people have different interests, and
sometimes it's difficult to reach consensus.
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In terms of where the major debates lie, there's
this distinction between mitochondria early and
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mitochondria late. And this space in the middle
of potentially mitochondria intermediate models,
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which I suppose we end up supporting. And it's
difficult to see, I suppose, how finally we
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might be able to resolve a lot of these questions.
But I think one thing that's changed in the field,
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in the, let's say, 15 years, I suppose, that
I've been working on the origin of eukaryotes,
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is that the models and the hypotheses that we have
now, they make predictions about organisms, which
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we might find in nature as we go exploring today.
So, for example, in the current paper,
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our analyses suggest that the archaeal host cell
underwent substantial complexification before
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the mitochondrial endosymbiosis. And nobody's
found archaea that are that complex in nature.
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The closest relatives of eukaryotes among the
archaea are very interesting, both in terms
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of their genomes and their cell biology. These
are the organisms called the Asgard archaea, and
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they've got some very interesting cell features,
like protrusions from the cell body, which might
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be used to interact with other organisms in the
environment. So potentially you could imagine
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how early interactions between the mitochondria
and the Asgard archaea could have occurred there.
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But they're really small, so they're typical
prokaryote size. And there's a huge mystery
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about how you go from two typically sized
prokaryotes, to something that's, you know, 100
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times or more larger. But I suppose our scenario
would suggest that perhaps if we keep looking,
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we will discover Asgards, which have yet more
of the sort of complexity that we associate with
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eukaryotes. And I suppose that sort of
environmental microbiology is the most
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promising way to find the hard evidence that
would really help us pin these things down.
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So, your work is really about the big evolutionary
questions. So, what gets you up in the morning?
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What excites you about what you're doing?
I suppose for me, this area of evolutionary
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work where you're using computational methods
to analyse biological data, genome data,
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that brings together for me two things that
I really like, which is, on the one hand,
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evolutionary theory, the processes of evolution,
how evolution works, and evolutionary history.
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And then, on the other hand, computers, and sort
of messing around with computers and programming.
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And those are two things that I've really
enjoyed for a long time. And I guess when I was
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an undergraduate, that's when I first realized
it would be possible to actually productively
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bring those together. That was at the time when
bioinformatics was developing as a field. So,
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writing some code to analyse genome data and
potentially coming to biological conclusions,
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it's really that that's always been
the most exciting thing for me.
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And the origin of eukaryotes is such a
great problem to work on because it's
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fundamentally important in understanding our
own evolutionary history. It's a topic that
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many people are interested in. It's a topic with
many very interesting ideas that can be tested.
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And it's also a topic that's often challenged us
to develop new methods that better capture how
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genomes evolve, to get better answers and more
accurate answers about how eukaryotes evolved.
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00:20:40,160
And the hope is that as we develop better models,
we learn about how genomes evolved the processes,
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and we can use those to better
understand evolutionary history.
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I think that's very exciting for me, yeah.
Tom, thank you so much for talking with me.
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This was a podcast by the Milner Centre
for Evolution at the University of Bath.
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I'm Turi King and thank you for listening.
If you have any thoughts or comments on
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00:21:04,960
this or any other episodes, please
contact us via our social media.
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00:21:09,075
For more information about the Milner Centre
for Evolution, you can visit our website.
