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      Amino acid fermentation at the origin of the genetic code

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      1 ,
      Biology Direct
      BioMed Central

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          Abstract

          There is evidence that the genetic code was established prior to the existence of proteins, when metabolism was powered by ribozymes. Also, early proto-organisms had to rely on simple anaerobic bioenergetic processes. In this work I propose that amino acid fermentation powered metabolism in the RNA world, and that this was facilitated by proto-adapters, the precursors of the tRNAs. Amino acids were used as carbon sources rather than as catalytic or structural elements. In modern bacteria, amino acid fermentation is known as the Stickland reaction. This pathway involves two amino acids: the first undergoes oxidative deamination, and the second acts as an electron acceptor through reductive deamination. This redox reaction results in two keto acids that are employed to synthesise ATP via substrate-level phosphorylation. The Stickland reaction is the basic bioenergetic pathway of some bacteria of the genus Clostridium. Two other facts support Stickland fermentation in the RNA world. First, several Stickland amino acid pairs are synthesised in abiotic amino acid synthesis. This suggests that amino acids that could be used as an energy substrate were freely available. Second, anticodons that have complementary sequences often correspond to amino acids that form Stickland pairs. The main hypothesis of this paper is that pairs of complementary proto-adapters were assigned to Stickland amino acids pairs. There are signatures of this hypothesis in the genetic code. Furthermore, it is argued that the proto-adapters formed double strands that brought amino acid pairs into proximity to facilitate their mutual redox reaction, structurally constraining the anticodon pairs that are assigned to these amino acid pairs. Significance tests which randomise the code are performed to study the extent of the variability of the energetic (ATP) yield. Random assignments can lead to a substantial yield of ATP and maintain enough variability, thus selection can act and refine the assignments into a proto-code that optimises the energetic yield. Monte Carlo simulations are performed to evaluate the establishment of these simple proto-codes, based on amino acid substitutions and codon swapping. In all cases, donor amino acids are assigned to anticodons composed of U+G, and have low redundancy (1-2 codons), whereas acceptor amino acids are assigned to the the remaining codons. These bioenergetic and structural constraints allow for a metabolic role for amino acids before their co-option as catalyst cofactors. Reviewers: this article was reviewed by Prof. William Martin, Prof. Eörs Szathmáry (nominated by Dr. Gáspár Jékely) and Dr. Ádám Kun (nominated by Dr. Sandor Pongor)

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          Most cited references51

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          Hydrothermal vents and the origin of life.

          Submarine hydrothermal vents are geochemically reactive habitats that harbour rich microbial communities. There are striking parallels between the chemistry of the H(2)-CO(2) redox couple that is present in hydrothermal systems and the core energy metabolic reactions of some modern prokaryotic autotrophs. The biochemistry of these autotrophs might, in turn, harbour clues about the kinds of reactions that initiated the chemistry of life. Hydrothermal vents thus unite microbiology and geology to breathe new life into research into one of biology's most important questions - what is the origin of life?
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            Ideas about atmospheric composition and climate on the early Earth have evolved considerably over the last 30 years, but many uncertainties still remain. It is generally agreed that the atmosphere contained little or no free oxygen initially and that oxygen concentrations increased markedly near 2.0 billion years ago, but the precise timing of and reasons for its rise remain unexplained. Likewise, it is usually conceded that the atmospheric greenhouse effect must have been higher in the past to offset reduced solar luminosity, but the levels of atmospheric carbon dioxide and other greenhouse gases required remain speculative. A better understanding of past atmospheric evolution is important to understanding the evolution of life and to predicting whether Earth-like planets might exist elsewhere in the galaxy.
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                Author and article information

                Journal
                Biol Direct
                Biol. Direct
                Biology Direct
                BioMed Central
                1745-6150
                2012
                10 February 2012
                : 7
                : 6
                Affiliations
                [1 ]Am Campus 1. Klosterneuburg A3400. Austria
                Article
                1745-6150-7-6
                10.1186/1745-6150-7-6
                3376031
                22325238
                7279bdc7-7dc3-4d64-b02b-b29b973cd7ba
                Copyright ©2012 de Vladar; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 November 2011
                : 10 February 2012
                Categories
                Hypothesis

                Life sciences
                Life sciences

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