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Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid

While mRNA stability has been demonstrated to control rates of translation, generating both global and local synonymous codon biases in many unicellular organisms, this explanation cannot adequately explain why codon bias strongly tracks neighboring intergene GC content; suggesting that structural d...

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Detalles Bibliográficos
Autores principales: Babbitt, Gregory A., Alawad, Mohammed A., Schulze, Katharina V., Hudson, André O.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4176184/
https://www.ncbi.nlm.nih.gov/pubmed/25200075
http://dx.doi.org/10.1093/nar/gku811
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author Babbitt, Gregory A.
Alawad, Mohammed A.
Schulze, Katharina V.
Hudson, André O.
author_facet Babbitt, Gregory A.
Alawad, Mohammed A.
Schulze, Katharina V.
Hudson, André O.
author_sort Babbitt, Gregory A.
collection PubMed
description While mRNA stability has been demonstrated to control rates of translation, generating both global and local synonymous codon biases in many unicellular organisms, this explanation cannot adequately explain why codon bias strongly tracks neighboring intergene GC content; suggesting that structural dynamics of DNA might also influence codon choice. Because minor groove width is highly governed by 3-base periodicity in GC, the existence of triplet-based codons might imply a functional role for the optimization of local DNA molecular dynamics via GC content at synonymous sites (≈GC3). We confirm a strong association between GC3-related intrinsic DNA flexibility and codon bias across 24 different prokaryotic multiple whole-genome alignments. We develop a novel test of natural selection targeting synonymous sites and demonstrate that GC3-related DNA backbone dynamics have been subject to moderate selective pressure, perhaps contributing to our observation that many genes possess extreme DNA backbone dynamics for their given protein space. This dual function of codons may impose universal functional constraints affecting the evolution of synonymous and non-synonymous sites. We propose that synonymous sites may have evolved as an ‘accessory’ during an early expansion of a primordial genetic code, allowing for multiplexed protein coding and structural dynamic information within the same molecular context.
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spelling pubmed-41761842014-12-01 Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid Babbitt, Gregory A. Alawad, Mohammed A. Schulze, Katharina V. Hudson, André O. Nucleic Acids Res Computational Biology While mRNA stability has been demonstrated to control rates of translation, generating both global and local synonymous codon biases in many unicellular organisms, this explanation cannot adequately explain why codon bias strongly tracks neighboring intergene GC content; suggesting that structural dynamics of DNA might also influence codon choice. Because minor groove width is highly governed by 3-base periodicity in GC, the existence of triplet-based codons might imply a functional role for the optimization of local DNA molecular dynamics via GC content at synonymous sites (≈GC3). We confirm a strong association between GC3-related intrinsic DNA flexibility and codon bias across 24 different prokaryotic multiple whole-genome alignments. We develop a novel test of natural selection targeting synonymous sites and demonstrate that GC3-related DNA backbone dynamics have been subject to moderate selective pressure, perhaps contributing to our observation that many genes possess extreme DNA backbone dynamics for their given protein space. This dual function of codons may impose universal functional constraints affecting the evolution of synonymous and non-synonymous sites. We propose that synonymous sites may have evolved as an ‘accessory’ during an early expansion of a primordial genetic code, allowing for multiplexed protein coding and structural dynamic information within the same molecular context. Oxford University Press 2014-09-29 2014-09-08 /pmc/articles/PMC4176184/ /pubmed/25200075 http://dx.doi.org/10.1093/nar/gku811 Text en © The Author(s) 2014. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Computational Biology
Babbitt, Gregory A.
Alawad, Mohammed A.
Schulze, Katharina V.
Hudson, André O.
Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid
title Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid
title_full Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid
title_fullStr Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid
title_full_unstemmed Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid
title_short Synonymous codon bias and functional constraint on GC3-related DNA backbone dynamics in the prokaryotic nucleoid
title_sort synonymous codon bias and functional constraint on gc3-related dna backbone dynamics in the prokaryotic nucleoid
topic Computational Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4176184/
https://www.ncbi.nlm.nih.gov/pubmed/25200075
http://dx.doi.org/10.1093/nar/gku811
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