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Sketches for a Mineral
Genetic Material
A. Graham Cairns-Smith1
I
will argue that the driving force for the transition from geochemistry
to biochemistry was natural selection operating, in its earliest stages,
on inorganic materials. The most critical requirement for truly primitive
evolvable systems is truly primitive genetic materials. These should have the
kind of permutable structure that can hold information, and they should
be able to replicate this information—very accurately for the most part.
They should be like DNA in these respects. But, unlike DNA, they must do it
all without any pre-evolved systems. Mixed-layer and polytypic materials
will be featured in attempts to sketch what we should be looking for.
KEYWORDS: origin of life, natural selection, takeover, mixed-layer, polytype, clays
INTRODUCTION
For an organic chemist, it is humbling to think about bacteria because these supposedly simplest of organisms are
amazingly good at doing organic chemistry. They can put
together molecules requiring many steps in their making.
Difficult, often huge molecules such as proteins are
churned out, thousands of different kinds of them, each a
characteristic constellation of some thousands of atoms
and with every atom connected up just so.
Such competence could only be a product of evolution
through natural selection. Yet for today’s organisms it is a
precondition too—for to take part in evolution, in today’s
way, a high organic-chemical competence is absolutely
required. This is the Fix we find ourselves in when we try to
think about the origin of it all. It is a Fix that arises, I think,
from the very nature of organic molecules, together with a
preconception that because they are so important now this
must have been so from the very beginning.
The Great Virtue and the Great Snag about
Organic Molecules as the Basis of Life
Organic molecules are ideal for highly evolved forms of life
(such as bacteria) if only because of the enormous number
of different molecules that can be made from a construction kit of atoms composed mainly of C, H, O, N, P, and S.
Extrapolating from results of Henze and Blair (1931), I concluded (1971, p. 2) that there are more possible ways to
connect 200 carbon atoms with 402 hydrogen atoms than
the number of electrons in the Universe, which according
to a famous estimate is about 1079 (Eddington 1935,
p. 221). And most protein molecules contain many more
atoms than 602, and more kinds of atoms too.
The Great Virtue of such richness in the world of possible
organic molecules is that it allows the kind of complex
1 Department of Chemistry, University of Glasgow, Glasgow,
G12 8QQ, Scotland
E-mail: [email protected]
ELEMENTS, VOL. 1,
PP.
157-161
molecular engineering found in all
the organisms around us now. The
Great Snag is that with so many
possibilities there are so very many
ways to go wrong—and end up
being a speck of dark intractable
tar instead of an exquisite piece of
sub-nano-engineering. To make
particular organic molecules,
detailed control is needed all the
way. In today’s organisms a crucial
part of this control is provided by
enzymes, which bring about virtually every biochemical reaction
taking place.
How Enzymes Work
An enzyme is a highly tuned molecular machine. It selects
and binds one or more particular molecule(s)—its “substrate”—from a diverse crowd of molecules in its surroundings. In the very act of binding, the enzyme exerts precise
forces on its substrate to transform it in a particular way.
An enzyme is mainly or entirely made of protein. It consists
of one or more chains of (usually) 20 kinds of amino acids,
covalently linked together in a definite sequence. A typical
chain might have some two or three hundred amino acids
in it, so that its unique sequence is one of an astronomical
number of alternatives (way beyond “the number of electrons in the Universe”). Often, such a protein chain folds
up in a complicated way that depends in detail on its
unique sequence. An enzyme protein may fold so as to create, somewhere on its surface, a specific groove or pit that
is geometrically and electronically complementary to the
molecule or molecules on which it acts. Enzyme and substrate fit together, and the fit becomes even better when the
substrate is distorted in ways that lead to the required reaction.
Such a set-up is indeed ideal for manipulation by Nature’s
engineer, natural selection. This is because the active site of
an enzyme—its critical “groove”—can be tuned by natural
selection. This can happen through occasional arbitrary
changes to a protein sequence arising from mutations in
the genetic material DNA. Such changes in or near the
groove would tend to make coarse adjustments to its shape
and chemical properties. Changes a bit farther away will
likely have smaller effects: perhaps moving components of
the groove by fractions of an angstrom, for fine tuning.
Similar considerations apply to other proteins. Yes, this
whole set-up is ideal for participation in evolution in the
way we now see it. But it is far from anything that might
have “just happened” as part of a primitive organic geochemistry. Manifestly, the situation that now allows the
evolution of organic-chemical competence must itself have
evolved. How did that happen? Our Fix has worsened with
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our increased understanding of the necessary complexities
of the biochemical machinery. We need to think about an
earlier phase of natural selection that did not in the first
place depend on high organic-chemical competence, but
could evolve to produce it. Is this feasible?
I think it is, but only if we abandon the idea that organic
molecules were always the stars in the play of evolution, as
they are today. Even the smallish molecules, amino acids,
and so on, owe their present significance to being parts of
incredibly high-tech machinery. What we are looking for
are low-tech beginners at evolution, and it is here that inorganic geochemistry is more likely to hold the keys.
SKETCHES
What are the minimal requirements for any system to be
subject to natural selection? The most basic is heredity,
illustrated in the well-known feature of living things that
they reproduce and pass on characteristics to offspring.
More strictly, what is passed on between generations is not
a set of characteristics as such (a phenotype), but genetic
information, which is the other, “invisible” part of an
organism. This is the information about how to make and
maintain a phenotype. It can be thought of as a set of controlling patterns—recipes of some sort (a genotype).
The first sketch, after Maynard Smith (1993), illustrates the
relationship between genotype and phenotype for the case
of (say) micro-organisms reproducing by cell division:
ä
P
ä
P
ä
P
ä
P′
ä
P′
à G à G à G à G′ à G′ à
MUTATION!
Phenotypes are not copies of previous phenotypes. On the
other hand, genotypes are usually accurate copies of previous genotypes—there is an unbroken succession of arrows
between the Gs. In addition there is the occasional mutation, which can be thought of as a “misprint” in the genetic
information. This will often produce a change in the phenotype which, if not too damaging, will be inherited from
then on.
Why Natural Selection is so Powerful
Mutations are effectively random events. But this is not to
say that because evolution depends on them, evolution
must be “just a matter of chance”. What makes natural
selection so much more effective than “pure chance” is that
it can proceed small-step-by-small-step—because partial
success is, in an important sense, remembered. Thus further
explorations can be made by randomly modifying what
was already successful—in the crucial self-demonstrating
sense of being more prevalent (surviving better, reproducing faster, spreading more widely, and so on) and so more
likely to be the basis of future random modifications. The
critical feature of the above diagram is the long-term memory, maintained through the accurate copying of genetic
information.
The next sketch, a modified version of the previous one,
emphasises where there had to be high competence from
the start (in the copying of the genetic information) and
where competence could have evolved later (in the production of phenotypes).
ä
P
ä
P
ä
P
ä
P′
ä
P′
è G è G è G è G′′ è G′′ è
MUTATION!
ELEMENTS
A phenotype can be seen in the most general terms as a set
of physico-chemical consequences of genetic patterns, consequences that affect the chances of the propagation of
these patterns. The consequences do not have to be anything very wonderful. To have a fair chance of catching on,
a phenotypic effect, even today, needs only to confer some
advantage even if small (Dawkins 1986).
Overcoming the Great Snag
Suppose the first genetic material was inorganic. We might
think of a microcrystalline mineral that has some replicable
pattern superimposed on its crystal structure, a pattern that
is inherited as a matter of course by newly crystallising
material. Now suppose that a consequence of such a pattern
is that it affects the morphology of the crystals holding it,
which in turn helps their survival and propagation.
FIGURE 1A is a cartoon example of how this might happen
and FIGURE 1B a conceivable case in point. Figure 1a illustrates the point that a first phenotype might simply be a
property of the genetic material itself (Spiegelman 1970;
Orgel 1979; Eigen 1983; Joyce 2002). But we can think too
about simple indirect phenotypic effects, involving nongenetic materials. Suppose that the replicable pattern of a
genetic crystal affects the population of ions and other
molecules that accumulate on or near its surfaces, altering
the local pH, perhaps, which in turn happens to favour the
growth of the genetic crystals. Or suppose that some replicable pattern has the effect of organising, just a little bit,
some mix of organic molecules in the surroundings,
through adsorptive and catalytic interactions. Adsorption
and catalysis are common-enough effects of inorganic surfaces, and “just a little bit” might be enough. For example
the crystallising materials might be clay minerals and the
organising effect might be to increase slightly the local
population of di- and/or tri-carboxylic acids, since these
can act as catalysts for clay synthesis by chelating and
mobilising insoluble ions, especially Al(III) (Siffert 1986).
Small di- and tri-carboxylic acids have a central place in our
biochemistry, and it has been suggested from the structure
of our present metabolic pathways that such acids were perhaps the very first organic molecules in our evolutionary
history (Hartman 1975; Cairns-Smith 1982, 1985, 2003).
But my main point here is that it is easy to imagine organic
molecules as primitive phenotypic components where even
rather disorganised mixtures might be effective. The great
trouble with the idea of organic molecules in an early
genetic role is illustrated by DNA, where clean and maintained supplies of DNA monomers (nucleotides) are the
absolute minimum requirements for its replication, and
nucleotides (whether for DNA or RNA) are particularly
tricky molecules to make (Cairns-Smith 1982, pp 56-59;
Shapiro 1988, 1995; Orgel 2004).
AN APPROACH TO G1
To be simple, and yet have a reasonably high information
capacity, a first genetic material should be made from a limited number of units that can be arranged in a very large
number of ways. DNA is like this. It holds its information
in the form of stacking sequences of tiny flat plates—base
pairs—held in place by an entwining pair of sugar–phosphate strings. There are two kinds of base pairs, and each
can be oriented in the stack in one of two ways.
The Power of Permutation
To get an idea of the amount of information that a structure like this can hold, consider this: a particular stack of
150 DNA base pairs is one arrangement out of about 1090
possible arrangements. And to get a rough idea of just how
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A Different Way of Replicating
A
Coming to the actual process of replication, this could be
very much simpler with “layer crystal genes” (as I will call
them) than with the necessarily highly orchestrated procedures of DNA replication, as I have discussed elsewhere
(1982). FIGURE 2 is a formal sketch of how such a crystal
gene might replicate a stacking sequence. The first requirement for such a mechanism is that units in the surrounding fluid should add only to the edges of the layer stacks,
and in such a way as not to disturb the sequence, indeed to
copy the sequence (Cairns-Smith 1988).
B
A mineral genetic material might hold information in the
form of a particular complex stacking sequence of layers
and replicate it through an appropriate alternation of growth and cleavage.
FIGURE 2
A. In this cartoon a ground water solution of silicic acid
and metal cations is moving through a porous medium
such as sandstone, and minerals such as clays or zeolites are crystallising from the solution. Crystals with chunky morphologies (A) would be
likely to block the pores and cut off local nutrient supplies, while crystals that are too small or delicate (B) would tend to wash away. A good
compromise would be to stick to the surrounding sand grains while not
blocking the pores (C).
FIGURE 1
B. This figure shows illite clay crystals from a marine sandstone, which
are conceivably a product of a simple kind of natural selection favouring crystals that stick to the sand grains while not blocking the pores
(see figure 1a). Such tapelike illites consist of small stacks of a few silicate layers. The inner layers are strongly negatively charged on both
their top and bottom surfaces, like mica, and are held together firmly
by (dry) potassium ions between them. However, the outer surfaces of
the top and bottom layers in a stack have a lower charge (more like
montmorillonite). These outer surfaces are hydrated and hold (hydrated) ions such as sodium and calcium (Nadeau et al. 1984). Micrograph
reproduced from McHardy et al. (1982).
far beyond the reaches of pure chance are all the forms of
life now on Earth, consider the bacterium E. coli. It has 4.6
million base pairs in its genotype. (Humans have a few hundred times as many, about 3.3 billion.)
What we seek is altogether more modest and certainly not
DNA. There are however some inorganic materials, including some clay minerals, that are formally like DNA in one
crucial respect: they consist of stacks of layers that are
either of different kinds (mixed-layer materials) or of different orientations (polytypes). In several cases, the layers
may be arranged in more or less arbitrary sequences. Such
materials could in principle hold information.
Furthermore, the conditions required for their synthesis—
for example, ground waters containing silicic acid and
metal cations—were most likely available on the primitive
Earth, as they are now (Odin et al. 1986).
ELEMENTS
Indirect support for this kind of faithful sideways copying
comes from a phenomenon sometimes seen in layer crystals where some complex random-looking block of layers is
repeated several times, one on top of the other. Examples
of this come from mixed-layer materials. Although formed
at high temperatures, barium ferrites have provided some
especially dramatic cases. For example, Kohn et al. (1971)
found a 526 Å repeating sequence of 37 layers, while in
another study McConnell et al. (1974) found an 841 Å
sequence of 59 layers. Each of these groups remarked that
limitations of their (different) electron microscope techniques may have prevented even longer repeating
sequences from being found. Clay minerals frequently have
mixed-layer structures and often show (more modest)
sequence repeats (Reynolds 1986). There is a similar story
with polytypes, e.g., silicon carbide (Verma and Krishna
1966) and micas (Baronnet 1980; Baronnet and Kang 1989).
The classical explanation for such repeats (Frank 1951) is
that the crystals would have grown through addition of
units to edges that are exposed on the surface due to a deep
screw dislocation. An alternative less tidy mechanism has
been suggested more recently (FIG. 3) to explain the long
repeats found in barium ferrites (Turner et al 1996). This
“seaweed growth” mechanism also depends on faithful
sideways addition of units. A similar mechanism might
apply to other cases of long c-axis repeats.
FIGURE 4 is a second sketch for an imagined mineral genetic
material. The picture is supposed to be part of one flexible,
branching, sprawling multi-layer (say, 10–100 layers thick)
and which has the same stacking sequence everywhere, displayed on its many edges like a vertical bar code. The whole
thing is somewhat like a plant reproducing vegetatively—as
happens with clover for example. One clone may eventual-
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And it is here, on the edge surfaces, that catalytic and
adsorptive sites would be most directly influenced by
sequence patterns. This might be possible—I am thinking
of those misfitting strains where, in the middle of a complicated sequence, there might be, say, an adjacent pair of
layers, A and B, which create a row of edge sites that
depend very much on the chemical nature of A and B and
how well they sit together. But these sites might depend
also, if more subtly, on the layers above and below them—
and so on, with the effects getting weaker with distance.
Transmission of such “mechanical” effects through articulated silicate structures has been discussed by Megaw et al.
(1962); see also Cairns-Smith (1982, p 223). This possibility, although speculative, is reminiscent of the evolutionary
“fine tuning” of protein catalysis discussed earlier.
Takeovers and the Evolution
of the Means to Evolve
A genetic takeover
Cartoon sketch illustrating a possible mechanism for
long repeat sequences quite often found in mixed-layer
crystals. A seed crystal (top left) consists of a stack of layers with some
arbitrary sequence. It grows by addition of units to its edges only (compare figure 2). The resulting more extensive plate is branched and flexible. It grows like seaweed so that “fronds” come to overlap and subsequently pile on top of each other producing thicker crystals in which
the original arbitrary sequence in the seed is repeated several times
(e.g., bottom right). The colour coding and numbering refer to different levels of the same stack of layers.
FIGURE 3
FIGURE 5 illustrates how an evolutionary process could
result in a radical change in genetic materials. No great leap
would be needed, only a gradual process with intermediate
stages in which evolving systems would use more than one
genetic material. This diagram represents a series of snapshots on a time scale of perhaps hundreds to millions of
years. It is the simplest form of a “genetic takeover”—
between just two genetic materials.
Formal representation of a radical genetic takeover. Here
phenotypes are represented as boxes, which protect the
genetic information and enable it to replicate more effectively. But they
let in the possibility of a new kind of genetic material (red) based on
materials that had not previously been available. After a period of collaboration the new system ousts the old.
FIGURE 5
FIGURE 4
An artist’s impression of a primitive mineral gene that
reproduces vegetatively (see figs 1b, 2, and 3b, and text).
ly spread over a whole field (Harper 1982). A sprawling
primitive gene like this could still evolve, if, for example, a
branch were to develop a stacking fault.
And its Phenotype?
Morphology could be a phenotypic feature (compare
fig. 1)— for example the thickness of the fronds, their style
of branching, their width—in so far as such features could
influence (say) accessibility of nutrient solutions or robustness to unfavourable conditions. Or perhaps undersaturated
conditions would allow small pieces to break off more easily if the width of a frond tended to vary along its length.
Particularly with mixed-layer structures (that is to say,
structures made from chemically different layers lying on
top of each other), there would be strains due to slight misfits that might tend to limit growth in certain directions or
cause curling. Such strains might affect the amount and
style of branching and hence the proportion of edges where
the genetic information is displayed. Indeed this whole
design with its flexible branching fronds increases the
prevalence of edges.
ELEMENTS
There are analogies here with human technological
advance where similar takeovers abound. The quill pen was
not gradually transformed into the word processing computer through a graded succession of intermediate designs,
but through an overlapping succession of takeovers using
novel technologies, each made possible by the evolution of
a whole surrounding technology. In more recent biological
evolution too there have been takeovers. Gills did not
evolve through intermediate designs into lungs—there was
a gradual takeover through organisms (such as lungfish)
that had both.
I think that takeovers would have had a special place at the
earliest stages of evolution. A series of genetic takeovers
could have provided the main mechanism for the evolution of the means to evolve—that is to say the evolution of
the genetic system itself. I also think that it was through an
overlapping succession of takeovers that different schemes
could have been tried out—simple ones to begin with,
more complicated ones becoming possible later.
A Genetic Staircase?
All the free-living organisms on Earth that we know of have
essentially the same highly integrated DNA-based system
that provides, now, the means to evolve. The implication
of this sameness is that all living creatures on Earth today,
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from bacteria to barley to bishops, are (in some sense)
descended from a single common ancestor that already had
this system in full working order with its fundamental features fixed, that is to say no longer subject to evolution.
Probably this arose from the kind of multiple interdependence of subsystems that is so typical of high-tech machinery in general (Cairns-Smith 1982, chapter 3).
Surely there must have been a prolonged or intensive evolution through natural selection to have brought such
machinery into existence. I would guess that this started
piecemeal with perhaps one kind of mineral genetic material, followed by several based on different kinds of mixedlayer or polytype materials: symbioses of several primitive
genetic materials with different evolved skills. FIGURE 6 is a
cartoon of the sort of thing I am trying to imagine here. It
is a kind of staircase showing roughly how lines of genetic
succession might have been arranged. The staircase has all
but collapsed now, but beginners like G1 should still be
with us engaging in, at least, tiny temporary evolutionary
processes. Perhaps these seem too trivial to be recognised
for what they are.
Hydrothermal systems might be the place to look. They are
being increasingly invoked as sites for “the origin of life”
(Holm 1992; Russell and Hall 1997), and they seem especially good places for the earliest stages of the kind of evolution we are trying to imagine. Layer silicates, for example,
grow and dissolve relatively quickly at moderately high
temperatures and pressures.
Finally, returning to the main theme of this essay, whatever
the detailed story was, there would not have been one fixed
set of materials all the way because the most accessible and
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ELEMENTS
A genetic staircase. The idea here is that there were multiple overlapping genetic takeovers. First there was one
genetic material. Then there were several doing different jobs. Finally
there was only DNA, which had become versatile enough in its means
of control (via proteins mainly) to do everything needed for its own
survival and propagation.
FIGURE 6
useful materials would change as the level of sophistication
rose. Above all, the whole process would have been transformed by the appearance of a competent organic chemistry, however that was achieved.
ACKNOWLEDGMENTS
I thank Bob Hazen for inviting me to contribute to this
issue of Elements and for encouraging my efforts. .
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