doi: 10.1371/journal.pcbi.1002024.
Epub 2011 Mar 24.
On the origin of DNA genomes: evolution of the division of labor between template and catalyst in model replicator systems
Affiliations
- PMID: 21455287
- PMCID: PMC3063752
- DOI: 10.1371/journal.pcbi.1002024
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On the origin of DNA genomes: evolution of the division of labor between template and catalyst in model replicator systems
PLoS Comput Biol.
2011 Mar.
Abstract
The division of labor between template and catalyst is a fundamental property of all living systems: DNA stores genetic information whereas proteins function as catalysts. The RNA world hypothesis, however, posits that, at the earlier stages of evolution, RNA acted as both template and catalyst. Why would such division of labor evolve in the RNA world? We investigated the evolution of DNA-like molecules, i.e. molecules that can function only as template, in minimal computational models of RNA replicator systems. In the models, RNA can function as both template-directed polymerase and template, whereas DNA can function only as template. Two classes of models were explored. In the surface models, replicators are attached to surfaces with finite diffusion. In the compartment models, replicators are compartmentalized by vesicle-like boundaries. Both models displayed the evolution of DNA and the ensuing division of labor between templates and catalysts. In the surface model, DNA provides the advantage of greater resistance against parasitic templates. However, this advantage is at least partially offset by the disadvantage of slower multiplication due to the increased complexity of the replication cycle. In the compartment model, DNA can significantly delay the intra-compartment evolution of RNA towards catalytic deterioration. These results are explained in terms of the trade-off between template and catalyst that is inherent in RNA-only replication cycles: DNA releases RNA from this trade-off by making it unnecessary for RNA to serve as template and so rendering the system more resistant against evolving parasitism. Our analysis of these simple models suggests that the lack of catalytic activity in DNA by itself can generate a sufficient selective advantage for RNA replicator systems to produce DNA. Given the widespread notion that DNA evolved owing to its superior chemical properties as a template, this study offers a novel insight into the evolutionary origin of DNA.
Conflict of interest statement
The authors have declared that no competing interests exist.
Figures
The notation is as follows: Rp and Dp denote RNA polymerase and DNA
polymerase respectively. The superscripts to Rp and Dp denote whether the
polymerase is in RNA-form (catalyst and template) or in DNA-form (template).
The prefixes to Rp and Dp denote the type of templates a polymerase depends
on: Rd stands for RNA-dependent, and Dd stands for DNA-dependent. Solid
arrows represent the template-product relationship. Broken arrows represent
the catalyst-reaction relationship. A: Self-replication system consists of
an RNA replicase (RdRp). B: Transcription system consists of a transcriptase
(DdRp) and a DNA replicase (DdDp). C: Reverse transcription system consists
of a transcriptase (DdRp) and a reverse transcriptase (RdDp).
The model was initialized such that the system consisted of a
population of RNA polymerase (Rp) and parasites. The simulation was
first run with the mutation converting Rp into Dp disabled
(
).
After the system reached evolutionary equilibrium (panel A), the
mutation was enabled (
), and
the resulting evolutionary dynamics are depicted in panel B to D.
The larger panels depict snapshots of simulations taken at different
times as indicated above panels. The color coding is indicated at
the bottom of the figure. RNA and DNA are not distinguished. The
timescale is scaled such that it has the same meaning as that of the
ordinary differential equation model that describes the replicator
dynamics with the same rate constants as in the CA model (the
timescale is scaled in this manner throughout the paper). The
smaller panels within the larger panels depict a two-dimensional
histogram of 
and
. See
the main text for the description for each panel. The parameters
(rate constants) used in this simulation were as follows:
(replication); 
(decay); 
(diffusion); 
(parasite advantage); 
(mutation rate of 
and
);
(mutation step); 
(mutation rate from Rp to Dp); 
(mutation rate to parasites). The size of CA was 1024×1024
squares. The boundary had no flux.
).
After the system reached evolutionary equilibrium (panel A), the
mutation was enabled (), and
the resulting evolutionary dynamics are depicted in panel B to D.
The larger panels depict snapshots of simulations taken at different
times as indicated above panels. The color coding is indicated at
the bottom of the figure. RNA and DNA are not distinguished. The
timescale is scaled such that it has the same meaning as that of the
ordinary differential equation model that describes the replicator
dynamics with the same rate constants as in the CA model (the
timescale is scaled in this manner throughout the paper). The
smaller panels within the larger panels depict a two-dimensional
histogram of and
. See
the main text for the description for each panel. The parameters
(rate constants) used in this simulation were as follows:
(replication);
(decay);
(diffusion);
(parasite advantage);
(mutation rate of and
);
(mutation step);
(mutation rate from Rp to Dp);
(mutation rate to parasites). The size of CA was 1024×1024
squares. The boundary had no flux.
The surface model was initialized such that the system consisted of
the transcription system (see below for the parameter values). No
mutation processes were enabled except for the mutation converting
molecules into parasite (
). The
color coding is indicated in the figure. The parameters were as
follows: 
and
for
both Rp and Dp; 
;
; the
size of CA was 512×512 squares; the other parameters were the
same as in Figure
2.
). The
color coding is indicated in the figure. The parameters were as
follows: and
for
both Rp and Dp; ;
; the
size of CA was 512×512 squares; the other parameters were the
same as in Figure
2.
After the surface model reached evolutionary equilibrium (Figure 2D), the
whole population of the RNA replicase (i.e. the self-replication
system) was removed from the system (Figure 4A), and the simulation
was continued. The resulting evolutionary dynamics are depicted
(Figure
4B–F). The figure has the same format as that of
Figure 2.
See the main text for the explanation of each panel. The parameters
where as follows: 
; the
size of CA was 512×512 squares; the other parameters were the
same as in Figure
2.
; the
size of CA was 512×512 squares; the other parameters were the
same as in Figure
2.
The surface model was initialized with a population of Rp (no
parasites were introduced in the system). The simulation was run in
the same manner as in Figure 2 with the mutation converting molecules into
parasites disabled (
). The
format of the figure is the same as that of Figure 2. For the explanation of
each panel, see the main text. The parameters were as follows:
; the
size of CA is 512×512 squares; the other parameters were the
same as in Figure
2.
). The
format of the figure is the same as that of Figure 2. For the explanation of
each panel, see the main text. The parameters were as follows:
; the
size of CA is 512×512 squares; the other parameters were the
same as in Figure
2.
Dual-Rp denotes a dual specificity Rp. In B, C and D, the
evolutionary dynamics progress from top to bottom. For the
explanation, see the main text.
The compartment model was initialized, and the simulation was run in
the same way as in Figure 2. The model was initialized such that the system
consisted of a population of Rp enclosed in a compartment. The
simulation was first run with the mutation converting Rp into Dp
disabled (
).
After the system reached evolutionary equilibrium (Figure 7A), the
mutation (
) was
enabled. The resulting evolutionary dynamics are depicted in panel B
to E. The left picture of each panel shows a snapshot of the
simulation taken at different times as indicated above panels. The
color coding is indicated in the upper left corner of the figure.
DNA and RNA are not distinguished. The insets depict two-dimensional
histogram of 
and
. The
right picture of each panel shows a snapshot with a different color
coding, which indicates the value of 
.
Distinction is not made between Dp and Rp and between DNA and RNA.
The insets depict a histogram of 
with
the same color coding as in the larger pictures that contain them.
For the explanation of each panel, see the main text. The parameters
were as follows: 
(the
volume threshold for division of compartments);
(the
target volume is set to the number of internal replicators
multiplied by 
);
; the
size of the CA is 512×512 squares; the other parameters were
the same as in Figure
2.
).
After the system reached evolutionary equilibrium (Figure 7A), the
mutation () was
enabled. The resulting evolutionary dynamics are depicted in panel B
to E. The left picture of each panel shows a snapshot of the
simulation taken at different times as indicated above panels. The
color coding is indicated in the upper left corner of the figure.
DNA and RNA are not distinguished. The insets depict two-dimensional
histogram of and
. The
right picture of each panel shows a snapshot with a different color
coding, which indicates the value of .
Distinction is not made between Dp and Rp and between DNA and RNA.
The insets depict a histogram of with
the same color coding as in the larger pictures that contain them.
For the explanation of each panel, see the main text. The parameters
were as follows: (the
volume threshold for division of compartments);
(the
target volume is set to the number of internal replicators
multiplied by );
; the
size of the CA is 512×512 squares; the other parameters were
the same as in Figure
2.
The figure depicts the same simulation and in the same format as in
Figure 7.
The time is reset to zero at an arbitrary moment after the time in
Figure 7E.
For the explanation of each panel, see the main text.
The model was modified such that interactions between molecules
happen globally regardless of the location of molecules (the system
is effectively well-mixed). The model was initialized with a
population of RpRNA in panel A, with a population of
RpRNA, RpDNA, DpRNA and
DpDNA in equal proportion in panel B and C, and with
a population of RpRNA, RpDNA and
DpRNA in equal proportion in panel D. The initial
value of Rrec and Drec were set as indicated in the figure (at
time = 0). The parameters were as follows:
(effectively); the size of the CA is
512×512 squares; the other parameters were the same as in
Figure
2.
(effectively); the size of the CA is
512×512 squares; the other parameters were the same as in
Figure
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