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Possible origin of life between mica sheets: does life imitate mica?
Helen Greenwood Hansma*
Department of Physics, University of California, Santa Barbara, CA 93106, USA
The mica hypothesis for the origin of life proposes that life originated between the sheets of muscovite mica. This paper
elaborates on two ways that life resembles what might have originated between mica sheets. First, enzymes: The cong-
urations and dynamics of enzymes, with their substrates, cofactors, and sometimes transition metal ions, often resemble
mica sheets, with their open-and-shut motions, acting on small molecules between them, sometimes assisted by transition
metal ions. Second, organisms: Mica world had the potential to be a community or ecosystem of prebiotic organisms in
a way unlike other models for the origin of life.
Keywords: muscovite; mechanochemistry; enzymes; protocells
*Email: hhansma@physics.ucsb.edu
Srinivasan & Morowitz, 2009; Wachtershauser, 2007). strands point alternately up and down. How did peptides
This ligand-assisted catalysis often involved transition evolve this alternating up-and-down structure in the rst
metal ions. Ligand-accelerated catalysis is highly enan- place? A single mineral surface would not foster this
tioselective. Ligands bound to a transition metal can bidirectional orientation. The structure that would foster
either speed up (catalyze) a reaction or slow it down this bidirectional orientation is a pair of mineral surfaces,
(Berrisford, Bolm, & Sharpless, 1995). The ligands cata- such as a pair of mica sheets. In todays life forms, beta
lyzing reactions are in complexes with transition metals. strands interact with adjacent beta strands to form paral-
Transition metal catalysts have been proposed as early lel and antiparallel beta sheets.
participants in the origin of life, because transition metals The disaccharide molecule between mica sheets, in
are essential parts of many enzymes. Transition metals Figure 3, also shows a possible advantage, for conning
are present as impurities in and between mica sheets. small biomolecules, of a mica sandwich, as compared
In the origin of life, many of the cofactors associated with a mineral surface or a swelling clay such as mont-
with enzymes today are believed to be the catalytic morillonite. The space between the mica sheets in Fig-
ligands that were involved with lifes origins. Several of ure 3 is 1 nm, while the spaces between sheets of
these cofactors are similar to nucleobases. These ligand swollen montmorillonite are 3 nm (Mathew & Luthey-
cofactors include various redox cofactors such as nicotin- Schulten, 2010). This disaccharide, mannose, has a twist
amide adenine dinucleotide (NAD+), NAD+ phosphate between the two monosaccharides. This would make it
(NADP+), avin adenine dinucleotide (FAD), and coen- likely to bind better to the surfaces of closely spaced
zyme A (CoA) (Wachtershauser, 1988, 2007). Flavin mica sheets than to wider-spaced mineral sheets or to a
mononucleotide (FMN), in Figure 5, is chemically single mineral surface.
related to FAD but has a simpler structure, lacking the
adenine. 2.3. Mica and clay minerals: nucleotide
These cofactors may have catalyzed specic classes polymerization
of reactions on surfaces (Wachtershauser, 1988). For Molecular dynamics (MD) simulations provide support
example, pyridoxal phosphate (PLP) is a cofactor in for micas possible role as a prebiotic enzyme. The clay
transamination reactions that acts by forming a labile mineral, montmorillonite, has been used as a catalyst and
Schiff base between its carbonyl group and the amino solid support for polymerizing activated nucleotides into
group to be transferred. Indeed, life appears to operate oligonucleotides (Ertem, 2004; Ferris, Aubrey, Liu, &
by catalyzing classes of reactions with specic types of Orgel, 1996). Exciting new MD simulations show that
enzymes: when a new enzyme is needed, an enzyme per- the spaces between clay sheets are better for catalyzing
forming the desired chemistry is recruited and modied polymerization reactions, as compared with their exposed
to bind the desired substrate (Petsko, Kenyon, Gerlt, surfaces (Mathew & Luthey-Schulten). Also, the correct
Ringe, & Kozarich, 1993). The alternate possibility biological polymerizations 35 linkages form pref-
appears not to be true: when a new enzyme is needed, erentially in the spaces between clay sheets, while unnat-
the enzyme that already binds the substrate to be modi- ural polymerizations with 55 linkages form
ed is not the enzyme that is modied to carry out the preferentially on the exposed surfaces.
desired chemistry. This is the conclusion of research on What does this have to do with a mica world? The
the origins of a rare and probably recent metabolic montmorillonite clay simulations should be applicable to
pathway in bacteria (Petsko et al., 1993). muscovite mica, because the clay and the mica have the
Cofactors between surfaces give more control of cat- same crystal structure and similar elemental composi-
alytic processes than cofactors on a single surface and tions, except for the cations in the interlayer, which are
the presence of two close-spaced surfaces connes the primarily Na+ for montmorillonite clay and K+ for
components of the reaction better than a single surface muscovite mica. The interlayer in the molecular dynam-
(Smith, Morowitz, & Copley, 2009). The spaces between ics simulations was water, with calcium ions, Ca++,
mica sheets thus provide an unusually structured micro- added for electrostatic and other reasons; neither Na+ nor
environment for solid state synthesis. The spaces K+ was present.
between mica sheets also provide an inorganic system Mica also has fewer crystal defects than montmoril-
that may be a precursor to the molecular motors of lonite, which is why it forms such large sheets instead of
living systems. being primarily in the form of clay. Therefore, the spaces
between mica sheets are likely to facilitate nucleotide
2.2. Peptides and saccharides polymerization, like the spaces between montmorillonite
Peptides are simple to synthesize, compared with nucleic sheets. Further analysis of mica vs. other minerals is
acids. This makes it likely that peptides were present in provided in Hansma (2010).
the earliest protolife. Beta strands are the most primitive Also, mica has an advantage over montmorillonite.
peptide structure. The amino acid side chains in beta In water, the spaces between sheets of montmorillonite
892 H.G. Hansma
swell to a separation of 3 nm. For comparison, the mica The spaces between mica sheets provide stable com-
sheets in the models of Figures 3 and 5 are only 1 nm partmentalization not possible with origins in vesicles,
apart. At the 3 nm separation of water-swollen montmo- which are labile, or in ponds, or on surfaces, or in swell-
rillonite clay, uridine monophosphate (UMP) binds to the ing clays. Thus, many types of prebiotic organisms
clay surface too weakly to diffuse in two dimensions on might have formed in the stable compartments of a mica
the clay surface. Mica does not swell in water. Instead, world that would not have formed elsewhere. Prebiotic
water slowly seeps in at the edges of the mica sheets, organisms in a mica world could be encapsulated in lipid
while the bulk of the sheet surface remains dry and membranes, which are stable on mica under aqueous
bridged by K+. This would keep the mica sheets closer uid (Hansma et al., 1991) and are probably also stable
together, at least in the region where the water ends and between mica sheets.
the mica sheets begin splitting. In mica, with its closer- Without compartmentalization, life would not be able
spaced sheets, UMP would remain closer to the mineral to develop a cell cycle or begin the process of speciation
surface, as compared with montmorillonite. In this case, (Adamala & Luisi, 2011). This reference proposes that
UMP might polymerize better, like AMP polymerizes the division of protocells was triggered either by some
between sheets of montmorillonite. inorganic catalyzing factor, such as porous surface, or
protocells divided when the encapsulated contents
reached some critical concentration. According to the
3. Mica world as an ecosystem of primitive organ- mica hypothesis, the division of protocells was triggered
isms by pressure from moving mica sheets, as in Figure 1.
The mica hypothesis describes actual prebiotic organ- Mica sheets may also have been the original cell
isms, where organism is dened as anything resem- walls. Cell walls surround all bacteria and archaea, as
bling a living creature in structure, behaviour, etc. A well as plant cells.
more detailed denition of such an organism is:
3.1. Geometry controls chemistry in nanoscale
any complex thing or system having properties and func- systems
tions determined not only by the properties and relations In the smallest compartments of living systems, such as
of its individual parts, but by the character of the whole cellular organelles, the kinetics of processes change with
that they compose and by the relations of the parts to
the whole. (http://dictionary.reference.com/browse/organ- changes in the shapes and volumes of the organelles (Liz-
ism) ana, Konkoli, Bauer, Jesorka, & Orwar, 2009). One rea-
son for this is that tiny changes in size or shape can cause
large changes in the concentrations of reactants, because
the volume depends on the cube of the radius, r3. This
assumes that water moves readily in and out of
compartments, while other molecules move slowly or not
at all.
Signal transduction can also occur as a result of size
changes, because size changes typically rearrange struc-
tures. Soft nanouidic systems often behave in similar
ways (Lizana et al., 2009).
Moving mica sheets would also be a system in which
geometry could control chemistry, for any reactant that
was associated with the surfaces of the mica sheets.
When mica sheets moved closer together, they would
partially enclose a smaller volume of uid within which
reactant would adsorb and desorb from the mica sheets.
When the mica sheets moved farther apart, they would
partially enclose a larger volume of uid within which
Figure 6. Mica provides massive redundancy and high error
tolerance. Error tolerance is high in the spaces between mica reactant would adsorb and desorb from the mica sheets.
sheets, as compared with prebiotic molecules in solution or on
surfaces. Therefore, almost everything can go wrong. Error 3.2. Error tolerance
tolerance is one of the main requirements for the origin of life. Almost everything will fail. Error tolerance is one of the
This diagram envisages a self-replicating ribozyme inhabiting main requirements for the origin of life (Dyson, 1999)
many spaces between mica sheets and diffusing in water to
other spaces between mica sheets. Much of this mica world
and is essential for the continued existence of life.
could be destroyed without eliminating all the molecules The hypothetical error tolerance of a mica world is
contained within it. illustrated in Figure 6. This error tolerance comes from
Origin of life between mica sheets 893
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