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Article: Natural selection retains overrepresented out-of-frame stop codons against frameshift peptides in prokaryotes

TitleNatural selection retains overrepresented out-of-frame stop codons against frameshift peptides in prokaryotes
Authors
Issue Date2010
PublisherBioMed Central Ltd. The Journal's web site is located at http://www.biomedcentral.com/bmcgenomics/
Citation
Bmc Genomics, 2010, v. 11 n. 1 How to Cite?
AbstractBackground: Out-of-frame stop codons (OSCs) occur naturally in coding sequences of all organisms, providing a mechanism of early termination of translation in incorrect reading frame so that the metabolic cost associated with frameshift events can be reduced. Given such a functional significance, we expect statistically overrepresented OSCs in coding sequences as a result of a widespread selection. Accordingly, we examined available prokaryotic genomes to look for evidence of this selection.Results: The complete genome sequences of 990 prokaryotes were obtained from NCBI GenBank. We found that low G+C content coding sequences contain significantly more OSCs and G+C content at specific codon positions were the principal determinants of OSC usage bias in the different reading frames. To investigate if there is overrepresentation of OSCs, we modeled the trinucleotide and hexanucleotide biases of the coding sequences using Markov models, and calculated the expected OSC frequencies for each organism using a Monte Carlo approach. More than 93% of 342 phylogenetically representative prokaryotic genomes contain excess OSCs. Interestingly the degree of OSC overrepresentation correlates positively with G+C content, which may represent a compensatory mechanism for the negative correlation of OSC frequency with G+C content. We extended the analysis using additional compositional bias models and showed that lower-order bias like codon usage and dipeptide bias could not explain the OSC overrepresentation. The degree of OSC overrepresentation was found to correlate negatively with the optimal growth temperature of the organism after correcting for the G+C% and AT skew of the coding sequence.Conclusions: The present study uses approaches with statistical rigor to show that OSC overrepresentation is a widespread phenomenon among prokaryotes. Our results support the hypothesis that OSCs carry functional significance and have been selected in the course of genome evolution to act against unintended frameshift occurrences. Some results also hint that OSC overrepresentation being a compensatory mechanism to make up for the decrease in OSCs in high G+C organisms, thus revealing the interplay between two different determinants of OSC frequency. © 2010 Tse et al; licensee BioMed Central Ltd.
Persistent Identifierhttp://hdl.handle.net/10722/157601
ISSN
2021 Impact Factor: 4.547
2020 SCImago Journal Rankings: 1.547
ISI Accession Number ID
Funding AgencyGrant Number
University of Hong Kong
Health, Welfare and Food Bureau
Funding Information:

We thank Tom Ho for his encouragement and comments during preparation of the manuscript. We acknowledge the support from the University Development Fund of the University of Hong Kong, and the HKSAR Research Fund for the Control of Infectious Diseases of the Health, Welfare and Food Bureau.

References

 

DC FieldValueLanguage
dc.contributor.authorTse, Hen_US
dc.contributor.authorCai, JJen_US
dc.contributor.authorTsoi, HWen_US
dc.contributor.authorLam, EPTen_US
dc.contributor.authorYuen, Ken_US
dc.date.accessioned2012-08-08T08:51:36Z-
dc.date.available2012-08-08T08:51:36Z-
dc.date.issued2010en_US
dc.identifier.citationBmc Genomics, 2010, v. 11 n. 1en_US
dc.identifier.issn1471-2164en_US
dc.identifier.urihttp://hdl.handle.net/10722/157601-
dc.description.abstractBackground: Out-of-frame stop codons (OSCs) occur naturally in coding sequences of all organisms, providing a mechanism of early termination of translation in incorrect reading frame so that the metabolic cost associated with frameshift events can be reduced. Given such a functional significance, we expect statistically overrepresented OSCs in coding sequences as a result of a widespread selection. Accordingly, we examined available prokaryotic genomes to look for evidence of this selection.Results: The complete genome sequences of 990 prokaryotes were obtained from NCBI GenBank. We found that low G+C content coding sequences contain significantly more OSCs and G+C content at specific codon positions were the principal determinants of OSC usage bias in the different reading frames. To investigate if there is overrepresentation of OSCs, we modeled the trinucleotide and hexanucleotide biases of the coding sequences using Markov models, and calculated the expected OSC frequencies for each organism using a Monte Carlo approach. More than 93% of 342 phylogenetically representative prokaryotic genomes contain excess OSCs. Interestingly the degree of OSC overrepresentation correlates positively with G+C content, which may represent a compensatory mechanism for the negative correlation of OSC frequency with G+C content. We extended the analysis using additional compositional bias models and showed that lower-order bias like codon usage and dipeptide bias could not explain the OSC overrepresentation. The degree of OSC overrepresentation was found to correlate negatively with the optimal growth temperature of the organism after correcting for the G+C% and AT skew of the coding sequence.Conclusions: The present study uses approaches with statistical rigor to show that OSC overrepresentation is a widespread phenomenon among prokaryotes. Our results support the hypothesis that OSCs carry functional significance and have been selected in the course of genome evolution to act against unintended frameshift occurrences. Some results also hint that OSC overrepresentation being a compensatory mechanism to make up for the decrease in OSCs in high G+C organisms, thus revealing the interplay between two different determinants of OSC frequency. © 2010 Tse et al; licensee BioMed Central Ltd.en_US
dc.languageengen_US
dc.publisherBioMed Central Ltd. The Journal's web site is located at http://www.biomedcentral.com/bmcgenomics/en_US
dc.relation.ispartofBMC Genomicsen_US
dc.titleNatural selection retains overrepresented out-of-frame stop codons against frameshift peptides in prokaryotesen_US
dc.typeArticleen_US
dc.identifier.emailTse, H:herman@graduate.hku.hken_US
dc.identifier.emailTsoi, HW:hwtsoi@hkucc.hku.hken_US
dc.identifier.emailYuen, K:kyyuen@hkucc.hku.hken_US
dc.identifier.authorityTse, H=rp00519en_US
dc.identifier.authorityTsoi, HW=rp00439en_US
dc.identifier.authorityYuen, K=rp00366en_US
dc.description.naturelink_to_subscribed_fulltexten_US
dc.identifier.doi10.1186/1471-2164-11-491en_US
dc.identifier.scopuseid_2-s2.0-77956477549en_US
dc.relation.referenceshttp://www.scopus.com/mlt/select.url?eid=2-s2.0-77956477549&selection=ref&src=s&origin=recordpageen_US
dc.identifier.volume11en_US
dc.identifier.issue1en_US
dc.identifier.eissn1471-2164-
dc.identifier.isiWOS:000282790900002-
dc.publisher.placeUnited Kingdomen_US
dc.identifier.scopusauthoridTse, H=7006070596en_US
dc.identifier.scopusauthoridCai, JJ=7403153560en_US
dc.identifier.scopusauthoridTsoi, HW=6603822102en_US
dc.identifier.scopusauthoridLam, EPT=36504245600en_US
dc.identifier.scopusauthoridYuen, K=36078079100en_US
dc.identifier.citeulike7822488-
dc.identifier.issnl1471-2164-

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