Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?

<p>Abstract</p> <p>Background</p> <p>The RNA world concept has wide, though certainly not unanimous, support within the origin-of-life scientific community. One view is that life may have emerged as early as the Hadean Eon 4.3-3.8 billion years ago with an atmosphere of...

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Main Authors: Bernhardt Harold S, Tate Warren P
Format: Article
Language:English
Published: BMC 2012-01-01
Series:Biology Direct
Subjects:
Online Access:http://www.biology-direct.com/content/7/1/4
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author Bernhardt Harold S
Tate Warren P
author_facet Bernhardt Harold S
Tate Warren P
author_sort Bernhardt Harold S
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>The RNA world concept has wide, though certainly not unanimous, support within the origin-of-life scientific community. One view is that life may have emerged as early as the Hadean Eon 4.3-3.8 billion years ago with an atmosphere of high CO<sub>2 </sub>producing an acidic ocean of the order of pH 3.5-6. Compatible with this scenario is the intriguing proposal that life arose within alkaline (pH 9-11) deep-sea hydrothermal vents like those of the 'Lost City', with the interface with the acidic ocean creating a proton gradient sufficient to drive the first metabolism. However, RNA is most stable at pH 4-5 and is unstable at alkaline pH, raising the possibility that RNA may have first arisen in the acidic ocean itself (possibly near an acidic hydrothermal vent), acidic volcanic lake or comet pond. As the Hadean Eon progressed, the ocean pH is inferred to have gradually risen to near neutral as atmospheric CO<sub>2 </sub>levels decreased.</p> <p>Presentation of the hypothesis</p> <p>We propose that RNA is well suited for a world evolving at acidic pH. This is supported by the enhanced stability at acidic pH of not only the RNA phosphodiester bond but also of the aminoacyl-(t)RNA and peptide bonds. Examples of <it>in vitro</it>-selected ribozymes with activities at acid pH have recently been documented. The subsequent transition to a DNA genome could have been partly driven by the gradual rise in ocean pH, since DNA has greater stability than RNA at alkaline pH, but not at acidic pH.</p> <p>Testing the hypothesis</p> <p>We have proposed mechanisms for two key RNA world activities that are compatible with an acidic milieu: <it>(i) </it>non-enzymatic RNA replication of a hemi-protonated cytosine-rich oligonucleotide, and <it>(ii) </it>specific aminoacylation of tRNA/hairpins through triple helix interactions between the helical aminoacyl stem and a single-stranded aminoacylating ribozyme.</p> <p>Implications of the hypothesis</p> <p>Our hypothesis casts doubt on the hypothesis that RNA evolved in the vicinity of alkaline hydrothermal vents. The ability of RNA to form protonated base pairs and triples at acidic pH suggests that standard base pairing may not have been a dominant requirement of the early RNA world.</p> <p>Reviewers</p> <p>This article was reviewed by Eugene Koonin, Anthony Poole and Charles Carter (nominated by David Ardell).</p>
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spelling doaj.art-191678daab89417ab222c66e2f3ef85f2022-12-22T03:07:10ZengBMCBiology Direct1745-61502012-01-0171410.1186/1745-6150-7-4Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?Bernhardt Harold STate Warren P<p>Abstract</p> <p>Background</p> <p>The RNA world concept has wide, though certainly not unanimous, support within the origin-of-life scientific community. One view is that life may have emerged as early as the Hadean Eon 4.3-3.8 billion years ago with an atmosphere of high CO<sub>2 </sub>producing an acidic ocean of the order of pH 3.5-6. Compatible with this scenario is the intriguing proposal that life arose within alkaline (pH 9-11) deep-sea hydrothermal vents like those of the 'Lost City', with the interface with the acidic ocean creating a proton gradient sufficient to drive the first metabolism. However, RNA is most stable at pH 4-5 and is unstable at alkaline pH, raising the possibility that RNA may have first arisen in the acidic ocean itself (possibly near an acidic hydrothermal vent), acidic volcanic lake or comet pond. As the Hadean Eon progressed, the ocean pH is inferred to have gradually risen to near neutral as atmospheric CO<sub>2 </sub>levels decreased.</p> <p>Presentation of the hypothesis</p> <p>We propose that RNA is well suited for a world evolving at acidic pH. This is supported by the enhanced stability at acidic pH of not only the RNA phosphodiester bond but also of the aminoacyl-(t)RNA and peptide bonds. Examples of <it>in vitro</it>-selected ribozymes with activities at acid pH have recently been documented. The subsequent transition to a DNA genome could have been partly driven by the gradual rise in ocean pH, since DNA has greater stability than RNA at alkaline pH, but not at acidic pH.</p> <p>Testing the hypothesis</p> <p>We have proposed mechanisms for two key RNA world activities that are compatible with an acidic milieu: <it>(i) </it>non-enzymatic RNA replication of a hemi-protonated cytosine-rich oligonucleotide, and <it>(ii) </it>specific aminoacylation of tRNA/hairpins through triple helix interactions between the helical aminoacyl stem and a single-stranded aminoacylating ribozyme.</p> <p>Implications of the hypothesis</p> <p>Our hypothesis casts doubt on the hypothesis that RNA evolved in the vicinity of alkaline hydrothermal vents. The ability of RNA to form protonated base pairs and triples at acidic pH suggests that standard base pairing may not have been a dominant requirement of the early RNA world.</p> <p>Reviewers</p> <p>This article was reviewed by Eugene Koonin, Anthony Poole and Charles Carter (nominated by David Ardell).</p>http://www.biology-direct.com/content/7/1/4RNA worldevolutionacidic pHprotonated base pairsRNA triple helixtRNA
spellingShingle Bernhardt Harold S
Tate Warren P
Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?
Biology Direct
RNA world
evolution
acidic pH
protonated base pairs
RNA triple helix
tRNA
title Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?
title_full Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?
title_fullStr Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?
title_full_unstemmed Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?
title_short Primordial soup or vinaigrette: did the RNA world evolve at acidic pH?
title_sort primordial soup or vinaigrette did the rna world evolve at acidic ph
topic RNA world
evolution
acidic pH
protonated base pairs
RNA triple helix
tRNA
url http://www.biology-direct.com/content/7/1/4
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