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Empirical demonstration of environmental sensing in catalytic RNA: evolution of interpretive behavior at the origins of life.

Lehman N, Bernhard T, Larson BC, Robinson AJ, Southgate CC - BMC Evol. Biol. (2014)

Bottom Line: Yet a variant of this sequence containing five mutations that alter its ability to utilize the Ca(2+) ion engenders a strong interpretive characteristic in this RNA.We have shown that RNA molecules in a test tube can meet the minimum criteria for the evolution of interpretive behaviour in regards to their responses to divalent metal ion concentrations in their environment.Interpretation in RNA molecules provides a property entirely dependent on natural physico-chemical interactions, but capable of shaping the evolutionary trajectory of macromolecules, especially in the earliest stages of life's history.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, Portland State University, Portland, OR, USA. niles@pdx.edu.

ABSTRACT

Background: The origins of life on the Earth required chemical entities to interact with their environments in ways that could respond to natural selection. The concept of interpretation, where biotic entities use signs in their environment as proxy for the existence of other items of selective value in their environment, has been proposed on theoretical grounds to be relevant to the origins and early evolution of life. However this concept has not been demonstrated empirically.

Results: Here, we present data that certain catalytic RNA sequences have properties that would enable interpretation of divalent cation levels in their environment. By assaying the responsiveness of two variants of the Tetrahymena ribozyme to the Ca(2+) ion as a sign for the more catalytically useful Mg(2+) ion, we show an empirical proof-of-principle that interpretation can be an evolvable trait in RNA, often suggested as a model system for early life. In particular we demonstrate that in vitro, the wild-type version of the Tetrahymena ribozyme is not interpretive, in that it cannot use Ca(2+) as a sign for Mg(2+). Yet a variant of this sequence containing five mutations that alter its ability to utilize the Ca(2+) ion engenders a strong interpretive characteristic in this RNA.

Conclusions: We have shown that RNA molecules in a test tube can meet the minimum criteria for the evolution of interpretive behaviour in regards to their responses to divalent metal ion concentrations in their environment. Interpretation in RNA molecules provides a property entirely dependent on natural physico-chemical interactions, but capable of shaping the evolutionary trajectory of macromolecules, especially in the earliest stages of life's history.

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Example payoff matrix for interpretive behaviour. Payoff values O1–O4 are evaluated for each pair-wise combination of environmental conditions and genotype traits as discussed in the text. The ion concentrations refer to those used in the assays of the Tetrahymena ribozyme, as described in Figures 2, 3 and 4.
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Fig1: Example payoff matrix for interpretive behaviour. Payoff values O1–O4 are evaluated for each pair-wise combination of environmental conditions and genotype traits as discussed in the text. The ion concentrations refer to those used in the assays of the Tetrahymena ribozyme, as described in Figures 2, 3 and 4.

Mentions: The simplest conceivable scenario in which an adaptive interpretive response could occur would involve a two-state entity in a two-state environment [5]. Suppose that the environment can be ‘favourable’ (F) or ‘unfavourable’ (U) and the entity has two possible states, A and B. Suppose further that in environment F it is advantageous for the entity to be in state A, and in environment U it is advantageous for the entity to be in state B. The overall ‘fitness’ of the entity in this varying environment may be expressed, by analogy with game theory, in terms of a 2×2 payoff matrix (Figure 1). There are four possible outcomes in the matrix: O1 (environment F, entity state A), O2 (environment U, entity state A), O3 (environment F, entity state B), and O4 (environment U, entity state B). The total ‘payoff’ (overall fitness) for the entity is the sum of O1 to O4, weighted according to the relative probabilities of each of these outcomes. In the non-interpretive configuration of the entity, its state (A or B) varies independently of the state of the environment. An interpretive variant of the entity might be capable of, say, responding to some sign that indicates (fallibly) that the state of the environment is F, the response being a change from state B to state A. This variant may have a selective advantage over the wildtype because it will increase the time that it spends in the advantageous combination of environment F and state A. Such interpretive responsiveness will only be adaptive, however, if it is not outweighed by the costs of a misinterpretation. This cost will be a function of the degree of disadvantage entailed by the entity being in state A in environment U, and the probability of being so placed in such a relation to the environment by the fallible (i.e., less than perfect) correlation between the presence of the sign and environmental state F.Figure 1


Empirical demonstration of environmental sensing in catalytic RNA: evolution of interpretive behavior at the origins of life.

Lehman N, Bernhard T, Larson BC, Robinson AJ, Southgate CC - BMC Evol. Biol. (2014)

Example payoff matrix for interpretive behaviour. Payoff values O1–O4 are evaluated for each pair-wise combination of environmental conditions and genotype traits as discussed in the text. The ion concentrations refer to those used in the assays of the Tetrahymena ribozyme, as described in Figures 2, 3 and 4.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4260251&req=5

Fig1: Example payoff matrix for interpretive behaviour. Payoff values O1–O4 are evaluated for each pair-wise combination of environmental conditions and genotype traits as discussed in the text. The ion concentrations refer to those used in the assays of the Tetrahymena ribozyme, as described in Figures 2, 3 and 4.
Mentions: The simplest conceivable scenario in which an adaptive interpretive response could occur would involve a two-state entity in a two-state environment [5]. Suppose that the environment can be ‘favourable’ (F) or ‘unfavourable’ (U) and the entity has two possible states, A and B. Suppose further that in environment F it is advantageous for the entity to be in state A, and in environment U it is advantageous for the entity to be in state B. The overall ‘fitness’ of the entity in this varying environment may be expressed, by analogy with game theory, in terms of a 2×2 payoff matrix (Figure 1). There are four possible outcomes in the matrix: O1 (environment F, entity state A), O2 (environment U, entity state A), O3 (environment F, entity state B), and O4 (environment U, entity state B). The total ‘payoff’ (overall fitness) for the entity is the sum of O1 to O4, weighted according to the relative probabilities of each of these outcomes. In the non-interpretive configuration of the entity, its state (A or B) varies independently of the state of the environment. An interpretive variant of the entity might be capable of, say, responding to some sign that indicates (fallibly) that the state of the environment is F, the response being a change from state B to state A. This variant may have a selective advantage over the wildtype because it will increase the time that it spends in the advantageous combination of environment F and state A. Such interpretive responsiveness will only be adaptive, however, if it is not outweighed by the costs of a misinterpretation. This cost will be a function of the degree of disadvantage entailed by the entity being in state A in environment U, and the probability of being so placed in such a relation to the environment by the fallible (i.e., less than perfect) correlation between the presence of the sign and environmental state F.Figure 1

Bottom Line: Yet a variant of this sequence containing five mutations that alter its ability to utilize the Ca(2+) ion engenders a strong interpretive characteristic in this RNA.We have shown that RNA molecules in a test tube can meet the minimum criteria for the evolution of interpretive behaviour in regards to their responses to divalent metal ion concentrations in their environment.Interpretation in RNA molecules provides a property entirely dependent on natural physico-chemical interactions, but capable of shaping the evolutionary trajectory of macromolecules, especially in the earliest stages of life's history.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, Portland State University, Portland, OR, USA. niles@pdx.edu.

ABSTRACT

Background: The origins of life on the Earth required chemical entities to interact with their environments in ways that could respond to natural selection. The concept of interpretation, where biotic entities use signs in their environment as proxy for the existence of other items of selective value in their environment, has been proposed on theoretical grounds to be relevant to the origins and early evolution of life. However this concept has not been demonstrated empirically.

Results: Here, we present data that certain catalytic RNA sequences have properties that would enable interpretation of divalent cation levels in their environment. By assaying the responsiveness of two variants of the Tetrahymena ribozyme to the Ca(2+) ion as a sign for the more catalytically useful Mg(2+) ion, we show an empirical proof-of-principle that interpretation can be an evolvable trait in RNA, often suggested as a model system for early life. In particular we demonstrate that in vitro, the wild-type version of the Tetrahymena ribozyme is not interpretive, in that it cannot use Ca(2+) as a sign for Mg(2+). Yet a variant of this sequence containing five mutations that alter its ability to utilize the Ca(2+) ion engenders a strong interpretive characteristic in this RNA.

Conclusions: We have shown that RNA molecules in a test tube can meet the minimum criteria for the evolution of interpretive behaviour in regards to their responses to divalent metal ion concentrations in their environment. Interpretation in RNA molecules provides a property entirely dependent on natural physico-chemical interactions, but capable of shaping the evolutionary trajectory of macromolecules, especially in the earliest stages of life's history.

Show MeSH