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Inferring gene function from evolutionary change in signatures of translation efficiency

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dc.contributor.author Krisko, Anita
dc.contributor.author Copic, Tea
dc.contributor.author Gabaldón Estevan, Juan Antonio, 1973-
dc.contributor.author Lehner, Ben, 1978-
dc.contributor.author Supek, Fran
dc.date.accessioned 2015-03-19T08:37:41Z
dc.date.available 2015-03-19T08:37:41Z
dc.date.issued 2014
dc.identifier.citation Krisko A, Copic T, Gabaldón T, Lehner B, Supek F. Inferring gene function from evolutionary change in signatures of translation efficiency. Genome Biology. 2014; 15: R44. DOI 10.1186/gb-2014-15-3-r44
dc.identifier.issn 1465-6906
dc.identifier.uri http://hdl.handle.net/10230/23225
dc.description.abstract Background: The genetic code is redundant, meaning that most amino acids can be encoded by more than one codon. Highly expressed genes tend to use optimal codons to increase the accuracy and speed of translation. Thus, codon usage biases provide a signature of the relative expression levels of genes, which can, uniquely, be quantified across the domains of life. Results: Here we describe a general statistical framework to exploit this phenomenon and to systematically associate genes with environments and phenotypic traits through changes in codon adaptation. By inferring evolutionary signatures of translation efficiency in 911 bacterial and archaeal genomes while controlling for confounding effects of phylogeny and inter-correlated phenotypes, we linked 187 gene families to 24 diverse phenotypic traits. A series of experiments in Escherichia coli revealed that 13 of 15, 19 of 23, and 3 of 6 gene families with changes in codon adaptation in aerotolerant, thermophilic, or halophilic microbes. Respectively, confer specific resistance to, respectively, hydrogen peroxide, heat, and high salinity. Further, we demonstrate experimentally that changes in codon optimality alone are sufficient to enhance stress resistance. Finally, we present evidence that multiple genes with altered codon optimality in aerobes confer oxidative stress resistance by controlling the levels of iron and NAD(P)H. Conclusions: Taken together, these results provide experimental evidence for a widespread connection between changes in translation efficiency and phenotypic adaptation. As the number of sequenced genomes increases, this novel genomic context method for linking genes to phenotypes based on sequence alone will become increasingly useful.
dc.description.sponsorship This work was supported by grants from the Spanish Ministry of Economy and Competitiveness (BFU2009-9618, BFU2008-00365 and ‘Centro de Excelencia Severo Ochoa 2013-2017’ SEV-2012-0208), an ERC Starting Grant, ERASysBio PLUS, AGAUR, the EMBO Young Investigator Program, and the EMBL-CRG Systems Biology Program. The work of FS was supported in part by Marie Curie Actions and by grant ICT-2013-612944 (MAESTRA). The experimental part of this work was carried out at and financed by the Mediterranean Institute for Life Sciences (MedILS)
dc.format.mimetype application/pdf
dc.language.iso eng
dc.publisher BioMed Central
dc.relation.ispartof Genome Biology. 2014; 15: R44
dc.rights © 2014 Krisko et al.; 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 credited.
dc.rights.uri http://creativecommons.org/licenses/by/2.0
dc.subject.other Seqüència d'aminoàcids
dc.subject.other Transcripció genètica
dc.title Inferring gene function from evolutionary change in signatures of translation efficiency
dc.type info:eu-repo/semantics/article
dc.identifier.doi http://dx.doi.org/10.1186/gb-2014-15-3-r44
dc.relation.projectID info:eu-repo/grantAgreement/ES/3PN/BFU2009-9618
dc.relation.projectID info:eu-repo/grantAgreement/ES/3PN/BFU2008-00365
dc.relation.projectID info:eu-repo/grantAgreement/ES/3PN/SEV-2012-0208
dc.rights.accessRights info:eu-repo/semantics/openAccess
dc.type.version info:eu-repo/semantics/publishedVersion

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