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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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Analyses of the interaction between interpretation and fitness for the PV ribozyme. Data are for reaction times of 5 minutes. (A) The parameter-space in which the probability of the presence of the sign (10 mM Ca2+) is 0.5 and the probability of the presence of 25 mM Mg2+ (as opposed to 0.5 mM Mg2+) varies from 0 to 1 (x-axis). The proportion of total product attributable to the interpretive component (I) of the ribozyme activity is shown on the y-axis. Four different scenarios from the total parameter space are illustrated, each with a different correlation coefficient (r) between the probability of the sign (10 mM Ca2+) and the probability of the favourable environment (25 mM Mg2+): r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). (B) The proportion of total activity of the PV ribozyme attributable to interpretation (y-axis) at varying probabilities of high (25 mM) Mg2+ (x-axis) with varying probabilities of the presence of the sign (10 mM Ca2+) and maximal correlation between the sign and the favourable environment (r = 1). Probability of the presence of the sign = 0.1 (closed circles), 0.3 (closed triangles), 0.5 (open triangles), 0.7 (open circles). For each of these curves a further set would be generated by lower levels of correlation, corresponding to the nest of curves in panel A. (C) Maximum available interpretive benefit (y-axis) at varying probabilities (x-axis) of the favourable environment (25 mM Mg2+) at various correlations (r) between the sign and the favourable environment: r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). Each calculated point corresponds to a peak on a member of the set of curves of which four are shown panel B.
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Fig5: Analyses of the interaction between interpretation and fitness for the PV ribozyme. Data are for reaction times of 5 minutes. (A) The parameter-space in which the probability of the presence of the sign (10 mM Ca2+) is 0.5 and the probability of the presence of 25 mM Mg2+ (as opposed to 0.5 mM Mg2+) varies from 0 to 1 (x-axis). The proportion of total product attributable to the interpretive component (I) of the ribozyme activity is shown on the y-axis. Four different scenarios from the total parameter space are illustrated, each with a different correlation coefficient (r) between the probability of the sign (10 mM Ca2+) and the probability of the favourable environment (25 mM Mg2+): r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). (B) The proportion of total activity of the PV ribozyme attributable to interpretation (y-axis) at varying probabilities of high (25 mM) Mg2+ (x-axis) with varying probabilities of the presence of the sign (10 mM Ca2+) and maximal correlation between the sign and the favourable environment (r = 1). Probability of the presence of the sign = 0.1 (closed circles), 0.3 (closed triangles), 0.5 (open triangles), 0.7 (open circles). For each of these curves a further set would be generated by lower levels of correlation, corresponding to the nest of curves in panel A. (C) Maximum available interpretive benefit (y-axis) at varying probabilities (x-axis) of the favourable environment (25 mM Mg2+) at various correlations (r) between the sign and the favourable environment: r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). Each calculated point corresponds to a peak on a member of the set of curves of which four are shown panel B.

Mentions: Figure 5a shows that, for the PV ribozyme, there is a positive interpretive component of fitness provided that there is a correlation between the presence of the sign (Ca2+) and the occurrence of the favourable environment (high concentration of Mg2+). As expected, the interpretive component of fitness rises with the degree of correlation between these variables.Figure 5


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)

Analyses of the interaction between interpretation and fitness for the PV ribozyme. Data are for reaction times of 5 minutes. (A) The parameter-space in which the probability of the presence of the sign (10 mM Ca2+) is 0.5 and the probability of the presence of 25 mM Mg2+ (as opposed to 0.5 mM Mg2+) varies from 0 to 1 (x-axis). The proportion of total product attributable to the interpretive component (I) of the ribozyme activity is shown on the y-axis. Four different scenarios from the total parameter space are illustrated, each with a different correlation coefficient (r) between the probability of the sign (10 mM Ca2+) and the probability of the favourable environment (25 mM Mg2+): r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). (B) The proportion of total activity of the PV ribozyme attributable to interpretation (y-axis) at varying probabilities of high (25 mM) Mg2+ (x-axis) with varying probabilities of the presence of the sign (10 mM Ca2+) and maximal correlation between the sign and the favourable environment (r = 1). Probability of the presence of the sign = 0.1 (closed circles), 0.3 (closed triangles), 0.5 (open triangles), 0.7 (open circles). For each of these curves a further set would be generated by lower levels of correlation, corresponding to the nest of curves in panel A. (C) Maximum available interpretive benefit (y-axis) at varying probabilities (x-axis) of the favourable environment (25 mM Mg2+) at various correlations (r) between the sign and the favourable environment: r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). Each calculated point corresponds to a peak on a member of the set of curves of which four are shown panel B.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
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Fig5: Analyses of the interaction between interpretation and fitness for the PV ribozyme. Data are for reaction times of 5 minutes. (A) The parameter-space in which the probability of the presence of the sign (10 mM Ca2+) is 0.5 and the probability of the presence of 25 mM Mg2+ (as opposed to 0.5 mM Mg2+) varies from 0 to 1 (x-axis). The proportion of total product attributable to the interpretive component (I) of the ribozyme activity is shown on the y-axis. Four different scenarios from the total parameter space are illustrated, each with a different correlation coefficient (r) between the probability of the sign (10 mM Ca2+) and the probability of the favourable environment (25 mM Mg2+): r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). (B) The proportion of total activity of the PV ribozyme attributable to interpretation (y-axis) at varying probabilities of high (25 mM) Mg2+ (x-axis) with varying probabilities of the presence of the sign (10 mM Ca2+) and maximal correlation between the sign and the favourable environment (r = 1). Probability of the presence of the sign = 0.1 (closed circles), 0.3 (closed triangles), 0.5 (open triangles), 0.7 (open circles). For each of these curves a further set would be generated by lower levels of correlation, corresponding to the nest of curves in panel A. (C) Maximum available interpretive benefit (y-axis) at varying probabilities (x-axis) of the favourable environment (25 mM Mg2+) at various correlations (r) between the sign and the favourable environment: r = 1 (closed circles), r = 0.75 (closed triangles), r = 0.5 (open triangles), r = 0.25 (open circles). Each calculated point corresponds to a peak on a member of the set of curves of which four are shown panel B.
Mentions: Figure 5a shows that, for the PV ribozyme, there is a positive interpretive component of fitness provided that there is a correlation between the presence of the sign (Ca2+) and the occurrence of the favourable environment (high concentration of Mg2+). As expected, the interpretive component of fitness rises with the degree of correlation between these variables.Figure 5

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