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Evolution of the division of labor between genes and enzymes in the RNA world.

Boza G, Szilágyi A, Kun Á, Santos M, Szathmáry E - PLoS Comput. Biol. (2014)

Bottom Line: Enzymatic activities of the two modeled ribozymes are in trade-off with their replication rates, and the relative replication rates compared to those of complementary strands are evolvable traits of the ribozymes.Although some asymmetry between gene and enzymatic strands could have evolved even in earlier, surface-bound systems, the shown mechanism in protocells seems inevitable and under strong positive selection.This could have preadapted the genetic system for transcription after the subsequent origin of chromosomes and DNA.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary; MTA-ELTE-MTMT Ecology Research Group, Budapest, Hungary.

ABSTRACT
The RNA world is a very likely interim stage of the evolution after the first replicators and before the advent of the genetic code and translated proteins. Ribozymes are known to be able to catalyze many reaction types, including cofactor-aided metabolic transformations. In a metabolically complex RNA world, early division of labor between genes and enzymes could have evolved, where the ribozymes would have been transcribed from the genes more often than the other way round, benefiting the encapsulating cells through this dosage effect. Here we show, by computer simulations of protocells harboring unlinked RNA replicators, that the origin of replicational asymmetry producing more ribozymes from a gene template than gene strands from a ribozyme template is feasible and robust. Enzymatic activities of the two modeled ribozymes are in trade-off with their replication rates, and the relative replication rates compared to those of complementary strands are evolvable traits of the ribozymes. The degree of trade-off is shown to have the strongest effect in favor of the division of labor. Although some asymmetry between gene and enzymatic strands could have evolved even in earlier, surface-bound systems, the shown mechanism in protocells seems inevitable and under strong positive selection. This could have preadapted the genetic system for transcription after the subsequent origin of chromosomes and DNA.

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Related in: MedlinePlus

The effect of degradation rate of macromolecules on strand asymmetry.The equilibrium ratio of the minus and plus strands (indicated by the heights as well as the colors of the bars; red: 0.9→yellow: 0.5) is not affected significantly by the rate of degradation, however increasing the degradation rate above a threshold results in the extinction of the replicators (notice the flat grey area on the right hand side of the graph). For strong trade-off (), this threshold is at a lower rate of degradation, whereas higher degradation rates are tolerated as the strength of trade-off decreases (). The results are averaged over 3 replicate model runs. Other parameters: , , , , , , , , ,  and .
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pcbi-1003936-g005: The effect of degradation rate of macromolecules on strand asymmetry.The equilibrium ratio of the minus and plus strands (indicated by the heights as well as the colors of the bars; red: 0.9→yellow: 0.5) is not affected significantly by the rate of degradation, however increasing the degradation rate above a threshold results in the extinction of the replicators (notice the flat grey area on the right hand side of the graph). For strong trade-off (), this threshold is at a lower rate of degradation, whereas higher degradation rates are tolerated as the strength of trade-off decreases (). The results are averaged over 3 replicate model runs. Other parameters: , , , , , , , , , and .

Mentions: High degradation rates can narrow the potential for the evolution of pronounced division of labor. Extreme trade-off between replication and metabolic activity selects for only few gene strands per protocell, hence a higher degradation rate easily eliminates them, and the few new genes synthesized from the ribozymes as templates may well suffer a similar fate: in the end the ribozymes cannot increase in number either, so all in all higher degradation rates lead to weaker admissible trade-off and result in weaker strand asymmetry (Figure 5). Larger protocells could, however, survive at higher degradation rates, potentially allowing for strand differentiation at strong trade-offs (the lower right part of Figure 5, where populations do not survive at the parameter values employed).


Evolution of the division of labor between genes and enzymes in the RNA world.

Boza G, Szilágyi A, Kun Á, Santos M, Szathmáry E - PLoS Comput. Biol. (2014)

The effect of degradation rate of macromolecules on strand asymmetry.The equilibrium ratio of the minus and plus strands (indicated by the heights as well as the colors of the bars; red: 0.9→yellow: 0.5) is not affected significantly by the rate of degradation, however increasing the degradation rate above a threshold results in the extinction of the replicators (notice the flat grey area on the right hand side of the graph). For strong trade-off (), this threshold is at a lower rate of degradation, whereas higher degradation rates are tolerated as the strength of trade-off decreases (). The results are averaged over 3 replicate model runs. Other parameters: , , , , , , , , ,  and .
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4256009&req=5

pcbi-1003936-g005: The effect of degradation rate of macromolecules on strand asymmetry.The equilibrium ratio of the minus and plus strands (indicated by the heights as well as the colors of the bars; red: 0.9→yellow: 0.5) is not affected significantly by the rate of degradation, however increasing the degradation rate above a threshold results in the extinction of the replicators (notice the flat grey area on the right hand side of the graph). For strong trade-off (), this threshold is at a lower rate of degradation, whereas higher degradation rates are tolerated as the strength of trade-off decreases (). The results are averaged over 3 replicate model runs. Other parameters: , , , , , , , , , and .
Mentions: High degradation rates can narrow the potential for the evolution of pronounced division of labor. Extreme trade-off between replication and metabolic activity selects for only few gene strands per protocell, hence a higher degradation rate easily eliminates them, and the few new genes synthesized from the ribozymes as templates may well suffer a similar fate: in the end the ribozymes cannot increase in number either, so all in all higher degradation rates lead to weaker admissible trade-off and result in weaker strand asymmetry (Figure 5). Larger protocells could, however, survive at higher degradation rates, potentially allowing for strand differentiation at strong trade-offs (the lower right part of Figure 5, where populations do not survive at the parameter values employed).

Bottom Line: Enzymatic activities of the two modeled ribozymes are in trade-off with their replication rates, and the relative replication rates compared to those of complementary strands are evolvable traits of the ribozymes.Although some asymmetry between gene and enzymatic strands could have evolved even in earlier, surface-bound systems, the shown mechanism in protocells seems inevitable and under strong positive selection.This could have preadapted the genetic system for transcription after the subsequent origin of chromosomes and DNA.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary; MTA-ELTE-MTMT Ecology Research Group, Budapest, Hungary.

ABSTRACT
The RNA world is a very likely interim stage of the evolution after the first replicators and before the advent of the genetic code and translated proteins. Ribozymes are known to be able to catalyze many reaction types, including cofactor-aided metabolic transformations. In a metabolically complex RNA world, early division of labor between genes and enzymes could have evolved, where the ribozymes would have been transcribed from the genes more often than the other way round, benefiting the encapsulating cells through this dosage effect. Here we show, by computer simulations of protocells harboring unlinked RNA replicators, that the origin of replicational asymmetry producing more ribozymes from a gene template than gene strands from a ribozyme template is feasible and robust. Enzymatic activities of the two modeled ribozymes are in trade-off with their replication rates, and the relative replication rates compared to those of complementary strands are evolvable traits of the ribozymes. The degree of trade-off is shown to have the strongest effect in favor of the division of labor. Although some asymmetry between gene and enzymatic strands could have evolved even in earlier, surface-bound systems, the shown mechanism in protocells seems inevitable and under strong positive selection. This could have preadapted the genetic system for transcription after the subsequent origin of chromosomes and DNA.

Show MeSH
Related in: MedlinePlus