Translational selection is ubiquitous in prokaryotes.
Codon usage bias in prokaryotic genomes is largely a consequence of background substitution patterns in DNA, but highly expressed genes may show a preference towards codons that enable more efficient and/or accurate translation. We introduce a novel approach based on supervised machine learning that...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2010-06-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC2891978?pdf=render |
| _version_ | 1818419483744665600 |
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| author | Fran Supek Nives Skunca Jelena Repar Kristian Vlahovicek Tomislav Smuc |
| author_facet | Fran Supek Nives Skunca Jelena Repar Kristian Vlahovicek Tomislav Smuc |
| author_sort | Fran Supek |
| collection | DOAJ |
| description | Codon usage bias in prokaryotic genomes is largely a consequence of background substitution patterns in DNA, but highly expressed genes may show a preference towards codons that enable more efficient and/or accurate translation. We introduce a novel approach based on supervised machine learning that detects effects of translational selection on genes, while controlling for local variation in nucleotide substitution patterns represented as sequence composition of intergenic DNA. A cornerstone of our method is a Random Forest classifier that outperformed previous distance measure-based approaches, such as the codon adaptation index, in the task of discerning the (highly expressed) ribosomal protein genes by their codon frequencies. Unlike previous reports, we show evidence that translational selection in prokaryotes is practically universal: in 460 of 461 examined microbial genomes, we find that a subset of genes shows a higher codon usage similarity to the ribosomal proteins than would be expected from the local sequence composition. These genes constitute a substantial part of the genome--between 5% and 33%, depending on genome size--while also exhibiting higher experimentally measured mRNA abundances and tending toward codons that match tRNA anticodons by canonical base pairing. Certain gene functional categories are generally enriched with, or depleted of codon-optimized genes, the trends of enrichment/depletion being conserved between Archaea and Bacteria. Prominent exceptions from these trends might indicate genes with alternative physiological roles; we speculate on specific examples related to detoxication of oxygen radicals and ammonia and to possible misannotations of asparaginyl-tRNA synthetases. Since the presence of codon optimizations on genes is a valid proxy for expression levels in fully sequenced genomes, we provide an example of an "adaptome" by highlighting gene functions with expression levels elevated specifically in thermophilic Bacteria and Archaea. |
| first_indexed | 2024-12-14T12:39:18Z |
| format | Article |
| id | doaj.art-bdeecb5dd3394343b0f1ace789c45a38 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-14T12:39:18Z |
| publishDate | 2010-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-bdeecb5dd3394343b0f1ace789c45a382022-12-21T23:00:58ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042010-06-0166e100100410.1371/journal.pgen.1001004Translational selection is ubiquitous in prokaryotes.Fran SupekNives SkuncaJelena ReparKristian VlahovicekTomislav SmucCodon usage bias in prokaryotic genomes is largely a consequence of background substitution patterns in DNA, but highly expressed genes may show a preference towards codons that enable more efficient and/or accurate translation. We introduce a novel approach based on supervised machine learning that detects effects of translational selection on genes, while controlling for local variation in nucleotide substitution patterns represented as sequence composition of intergenic DNA. A cornerstone of our method is a Random Forest classifier that outperformed previous distance measure-based approaches, such as the codon adaptation index, in the task of discerning the (highly expressed) ribosomal protein genes by their codon frequencies. Unlike previous reports, we show evidence that translational selection in prokaryotes is practically universal: in 460 of 461 examined microbial genomes, we find that a subset of genes shows a higher codon usage similarity to the ribosomal proteins than would be expected from the local sequence composition. These genes constitute a substantial part of the genome--between 5% and 33%, depending on genome size--while also exhibiting higher experimentally measured mRNA abundances and tending toward codons that match tRNA anticodons by canonical base pairing. Certain gene functional categories are generally enriched with, or depleted of codon-optimized genes, the trends of enrichment/depletion being conserved between Archaea and Bacteria. Prominent exceptions from these trends might indicate genes with alternative physiological roles; we speculate on specific examples related to detoxication of oxygen radicals and ammonia and to possible misannotations of asparaginyl-tRNA synthetases. Since the presence of codon optimizations on genes is a valid proxy for expression levels in fully sequenced genomes, we provide an example of an "adaptome" by highlighting gene functions with expression levels elevated specifically in thermophilic Bacteria and Archaea.http://europepmc.org/articles/PMC2891978?pdf=render |
| spellingShingle | Fran Supek Nives Skunca Jelena Repar Kristian Vlahovicek Tomislav Smuc Translational selection is ubiquitous in prokaryotes. PLoS Genetics |
| title | Translational selection is ubiquitous in prokaryotes. |
| title_full | Translational selection is ubiquitous in prokaryotes. |
| title_fullStr | Translational selection is ubiquitous in prokaryotes. |
| title_full_unstemmed | Translational selection is ubiquitous in prokaryotes. |
| title_short | Translational selection is ubiquitous in prokaryotes. |
| title_sort | translational selection is ubiquitous in prokaryotes |
| url | http://europepmc.org/articles/PMC2891978?pdf=render |
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