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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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Proposed evolutionary progression of interpretation in theTetrahymenaribozyme system. At or near the origins of life on the Earth 4 Ga, there were no catalytic RNAs with any interpretive ability. Selection for interpretation in a relatively calcium-rich but magnesium poor environment (Table 3) drove the advent of RNAs akin to the PV, which used Ca2+ as a sign for the preferred Mg2+ ion. As the abiotic and biotic environments evolved to sequester Mg2+ + ions in cells, the advantage to interpretation waned, and in contemporary cells relatively enriched in Mg2+ + RNAs such as the CG evolved under pressures to maximize their use of Mg2+.
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Fig6: Proposed evolutionary progression of interpretation in theTetrahymenaribozyme system. At or near the origins of life on the Earth 4 Ga, there were no catalytic RNAs with any interpretive ability. Selection for interpretation in a relatively calcium-rich but magnesium poor environment (Table 3) drove the advent of RNAs akin to the PV, which used Ca2+ as a sign for the preferred Mg2+ ion. As the abiotic and biotic environments evolved to sequester Mg2+ + ions in cells, the advantage to interpretation waned, and in contemporary cells relatively enriched in Mg2+ + RNAs such as the CG evolved under pressures to maximize their use of Mg2+.

Mentions: The evolutionary scenario that we envisage from these results describes at least three distinct temporal stages (Figure 6). The first stage would be that of primordial, nearly random, and simple RNA sequences not optimized for replicative activity by natural selection. These RNAs would take advantage of the dominant divalent cation in their environment (Ca2+) to facilitate catalysis [19]. The binding would have been weak and many RNA sequences would have been able to conform to the binding of the relatively large and diffuse Ca2+ ion; but any anionic backbone shielding and/or catalytic prowess provided by this ion would have been potentially beneficial. Here the Ca2+ ion would have been the object itself, and not a sign.Figure 6


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)

Proposed evolutionary progression of interpretation in theTetrahymenaribozyme system. At or near the origins of life on the Earth 4 Ga, there were no catalytic RNAs with any interpretive ability. Selection for interpretation in a relatively calcium-rich but magnesium poor environment (Table 3) drove the advent of RNAs akin to the PV, which used Ca2+ as a sign for the preferred Mg2+ ion. As the abiotic and biotic environments evolved to sequester Mg2+ + ions in cells, the advantage to interpretation waned, and in contemporary cells relatively enriched in Mg2+ + RNAs such as the CG evolved under pressures to maximize their use of Mg2+.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Proposed evolutionary progression of interpretation in theTetrahymenaribozyme system. At or near the origins of life on the Earth 4 Ga, there were no catalytic RNAs with any interpretive ability. Selection for interpretation in a relatively calcium-rich but magnesium poor environment (Table 3) drove the advent of RNAs akin to the PV, which used Ca2+ as a sign for the preferred Mg2+ ion. As the abiotic and biotic environments evolved to sequester Mg2+ + ions in cells, the advantage to interpretation waned, and in contemporary cells relatively enriched in Mg2+ + RNAs such as the CG evolved under pressures to maximize their use of Mg2+.
Mentions: The evolutionary scenario that we envisage from these results describes at least three distinct temporal stages (Figure 6). The first stage would be that of primordial, nearly random, and simple RNA sequences not optimized for replicative activity by natural selection. These RNAs would take advantage of the dominant divalent cation in their environment (Ca2+) to facilitate catalysis [19]. The binding would have been weak and many RNA sequences would have been able to conform to the binding of the relatively large and diffuse Ca2+ ion; but any anionic backbone shielding and/or catalytic prowess provided by this ion would have been potentially beneficial. Here the Ca2+ ion would have been the object itself, and not a sign.Figure 6

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
Related in: MedlinePlus