The Effect of Environment on the Evolution and Proliferation of Protocells of Increasing Complexity

Abstract

The formation, growth, division and proliferation of protocells containing RNA strands is an important step in ensuring the viability of a mixed RNA-lipid world. Experiments and computer simulations indicate that RNA encapsulated inside protocells can favor the protocell, promoting its growth while protecting the system from being over-run by selfish RNA sequences. Recent work has also shown that the rolling-circle replication mechanism can be harnessed to ensure the rapid growth of RNA strands and the probabilistic emergence and proliferation of protocells with functionally diverse ribozymes. Despite these advances in our understanding of a primordial RNA-lipid world, key questions remain about the ideal environment for the formation of protocells and its role in regulating the proliferation of functionally complex protocells. The hot spring hypothesis suggests that mineral-rich regions near hot springs, subject to dry-wet cycles, provide an ideal environment for the origin of primitive protocells. We develop a computational model to study protocellular evolution in such environments that are distinguished by the occurrence of three distinct phases, a wet phase, followed by a gel phase, and subsequently by a dry phase. We determine the conditions under which protocells containing multiple types of ribozymes can evolve and proliferate in such regions. We find that diffusion in the gel phase can inhibit the proliferation of complex protocells with the extent of inhibition being most significant when a small fraction of protocells is eliminated during environmental cycling. Our work clarifies how the environment can shape the evolution and proliferation of complex protocells.

Keywords: RNA world; evolution; hot spring hypothesis; origin of life; primordial environment; protocell; ribozymes.

Figure 1

(A) Pictorial representation of the three phases that periodically occur in hot spring environments. Multilamellar structures can form on mineral surfaces from lipid molecules in the dry phase, one layer of which is represented as a 2D lattice containing sites for RNA polymerization. Each site can swell into a vesicle in the wet phase. In the gel phase, the vesicles become deposited on the 2D surface and their membranes start to fuse, creating channels between them that can allow for the long-range diffusion of large RNA strands. Subsequent to this stage, the multilamellar structure forms again in the next dry phase. (B) Three-dimensional (3D) representation of the formation of vesicles from the lamella in the wet phase.

Figure 2

Time evolution plots (1 trial each) showing the percentage of sites containing all 4 types of ribozymes for $D=0\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ (blue); $D=0.00128\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ (orange) and $D=1.28\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ (green) starting from 1 circular ssRNA per site initially.

Figure 3

Time evolution of the fraction of empty sites for $D=0\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ with no protocell degradation in the wet phase; $D=0\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ when protocells degrade with probability $P_{kill}=0.01$; $D=0\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ when protocells degrade with probability $P_{kill}=0.02$; $D=1.28\mathsf{\mu }{\mathrm{m}}^2{\mathrm{h}}^{-1}$ when protocells degrade with probability $P_{kill}=0.01$.

Figure 4

Total number of RNA strands vs. time for a site having a low $K_{rep}$ value of the initial template and its eight neighboring sites for the case when protocells can degrade in the wet phase with probability $P_{kill}=0.01$. In this figure, the plots for those 9 sites are arranged in a manner that is identical to their arrangements on the lattice; i.e., the plot in row 2, column 2 corresponds to the central site and the sub-plots surrounding it correspond to its 8 neighbors.

Figure 5

Number of cyclases vs. time for sites corresponding to panels in (A) row 1, column 1, (B) row 2, column 2 and (C) row 2, column 1; shown in Figure 4.

Figure 6

Expansion of protocell population from only one site containing 5 circular ssRNA templates initially. (A) Initial stage; (B) intermediate stage (on the 300th day) and (C) when the percentage of sites with all 4 ribozymes becomes 90%. Color values: Black: $0\to$ no strands, Purple: $1\to$ contains only non-enzymatic strands, Magenta: $2\to$ contains 1 type of ribozyme, Orange: $3\to$ contains 2 types of ribozymes, Dark Yellow: $4\to$ contains 3 types of ribozymes, Light Yellow: $5\to$ contains 4 types of ribozymes.