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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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TheTetrahymenaribozymes, with secondary structures modified from [10]. The L–21 (‘length minus 21’ nucleotides from the 5′ end of the in vivo intron) sequence is shown for the wild-type ribozyme, with the five mutations in the CaCl2-competent variant (PV) [12] indicated by the circles: A103G, A187U, A270G, U271C, and G312A. Numbering scheme follows the original [8,11,12], with dots provided every ten nucleotides. The interaction between the internal guide sequence (IGS) and six nucleotides of the substrate is shown by the grey box; in the ‘pick-up-the-tail’ assay the hydroxyl of the 3′ nucleotide (G414, shown) attacks at the splice site in the substrate (lower-case letters) and transfers the 3′ portion of the substrate (the last 17 nucleotides of S-1t in this case = AAAUAAAUAAAUAAAUA) to the 3′ end of the ribozyme, thereby lengthening it making it detectable by gel electrophoretic analysis. In this drawing, 71 nucleotide near the 3′ end of the ribozyme were omitted for clarity. Bars between nucleotide pairs denote canonical Watson-Crick pairs, while dots denote non-canonical base-paring interactions. The active site of this ribozyme is the environment around the G414 and the stack of base-triples that is above and below it [13].
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Fig2: TheTetrahymenaribozymes, with secondary structures modified from [10]. The L–21 (‘length minus 21’ nucleotides from the 5′ end of the in vivo intron) sequence is shown for the wild-type ribozyme, with the five mutations in the CaCl2-competent variant (PV) [12] indicated by the circles: A103G, A187U, A270G, U271C, and G312A. Numbering scheme follows the original [8,11,12], with dots provided every ten nucleotides. The interaction between the internal guide sequence (IGS) and six nucleotides of the substrate is shown by the grey box; in the ‘pick-up-the-tail’ assay the hydroxyl of the 3′ nucleotide (G414, shown) attacks at the splice site in the substrate (lower-case letters) and transfers the 3′ portion of the substrate (the last 17 nucleotides of S-1t in this case = AAAUAAAUAAAUAAAUA) to the 3′ end of the ribozyme, thereby lengthening it making it detectable by gel electrophoretic analysis. In this drawing, 71 nucleotide near the 3′ end of the ribozyme were omitted for clarity. Bars between nucleotide pairs denote canonical Watson-Crick pairs, while dots denote non-canonical base-paring interactions. The active site of this ribozyme is the environment around the G414 and the stack of base-triples that is above and below it [13].

Mentions: 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.


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)

TheTetrahymenaribozymes, with secondary structures modified from [10]. The L–21 (‘length minus 21’ nucleotides from the 5′ end of the in vivo intron) sequence is shown for the wild-type ribozyme, with the five mutations in the CaCl2-competent variant (PV) [12] indicated by the circles: A103G, A187U, A270G, U271C, and G312A. Numbering scheme follows the original [8,11,12], with dots provided every ten nucleotides. The interaction between the internal guide sequence (IGS) and six nucleotides of the substrate is shown by the grey box; in the ‘pick-up-the-tail’ assay the hydroxyl of the 3′ nucleotide (G414, shown) attacks at the splice site in the substrate (lower-case letters) and transfers the 3′ portion of the substrate (the last 17 nucleotides of S-1t in this case = AAAUAAAUAAAUAAAUA) to the 3′ end of the ribozyme, thereby lengthening it making it detectable by gel electrophoretic analysis. In this drawing, 71 nucleotide near the 3′ end of the ribozyme were omitted for clarity. Bars between nucleotide pairs denote canonical Watson-Crick pairs, while dots denote non-canonical base-paring interactions. The active site of this ribozyme is the environment around the G414 and the stack of base-triples that is above and below it [13].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig2: TheTetrahymenaribozymes, with secondary structures modified from [10]. The L–21 (‘length minus 21’ nucleotides from the 5′ end of the in vivo intron) sequence is shown for the wild-type ribozyme, with the five mutations in the CaCl2-competent variant (PV) [12] indicated by the circles: A103G, A187U, A270G, U271C, and G312A. Numbering scheme follows the original [8,11,12], with dots provided every ten nucleotides. The interaction between the internal guide sequence (IGS) and six nucleotides of the substrate is shown by the grey box; in the ‘pick-up-the-tail’ assay the hydroxyl of the 3′ nucleotide (G414, shown) attacks at the splice site in the substrate (lower-case letters) and transfers the 3′ portion of the substrate (the last 17 nucleotides of S-1t in this case = AAAUAAAUAAAUAAAUA) to the 3′ end of the ribozyme, thereby lengthening it making it detectable by gel electrophoretic analysis. In this drawing, 71 nucleotide near the 3′ end of the ribozyme were omitted for clarity. Bars between nucleotide pairs denote canonical Watson-Crick pairs, while dots denote non-canonical base-paring interactions. The active site of this ribozyme is the environment around the G414 and the stack of base-triples that is above and below it [13].
Mentions: 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.

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