Cited by 262RNA and protein synthesis mechanismsBacterial Genetics and BiotechnologyGenomics and Phylogenetic Studies

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Nonrandom utilization of codon pairs in Escherichia coli.

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Gutman, G A, Hatfield, G W·1989·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.86.10.3699PMC PMC287207

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Abstract

We have analyzed protein-coding sequences of Escherichia coli and find that codon-pair utilization is highly biased, reflecting overrepresentation or underrepresentation of many pairs compared with their random expectations. This effect is over and above that contributed by nonrandomness in the use of amino acid pairs, which itself is highly evident; it is much weaker when nonadjacent codon pairs are examined and virtually disappears when pairs separated by two or three intervening codons are evaluated. There appears to be a high degree of directionality in this bias: any codon that participates in many nonrandom pairs tends to make both over- and underrepresented pairs, but preferentially as a left- or right-hand member. We show a relationship between codon-pair utilization patterns and levels of gene expression: genes encoding proteins expressed at high levels tend to contain more abundant, but more highly underrepresented, codon pairs, relative to genes expressed at low levels. The nonrandom utilization of codon pairs may be a consequence of their effects on translational efficiency, which in turn may be related to the compatibility of adjacent aminoacyl-tRNA isoacceptors at the A and P sites of a translating ribosome.

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Background
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Background
Frameshift and wild-type proteins are highly similar because the genetic code and genomes were optimized for frameshift tolerancePreprint
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Background
The shiftability of protein coding genes: the genetic code was optimized for frameshift toleratingPreprint
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“It has been widely reported that the usage of codon pairs are highly biased in various species, including virus, bacteria, human and animals [25, 27-32].”
Method
Improving the accuracy of recombinant protein production through integration of bioinformatics, statistical and mass spectrometry methodologies
Ragionieri, L., Vitorino, R. M. P., Frommlet, J. C., Oliveira, J. L., Gaspar, P., de Pouplana, L. R., Santos, M. A. S., & Moura, G. R. (2014) · FEBS Journal · doi:10.1111/febs.13181 · Cited by 11
“Codon context (CC) refers to non-random utilization of adjacent codon pairs [14 – 16], and relates to tRNA/tRNA steric interaction in the ribosomes [17,18] that inﬂuence the translation elongation rate and accuracy in Escherichia coli [16,19,20].”
Background
Genetic evolution and codon usage analysis of NKX-2.5 gene governing heart development in some mammals
Malakar, A. K., Halder, B., Paul, P., et al. (2019) · Genomics · doi:10.1016/j.ygeno.2019.07.023 · Cited by 11
Pairs of amino acids at the P- and A-sites of the ribosome predictably and causally modulate translation-elongation rates
Ahmed, N., Friedrich, U. A., Sormanni, P., Ciryam, P., Altman, N., Bukau, B., Krämer, G., & O’Brien, E. P. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.10.030 · Cited by 11
RecBCD enzyme and Chi recombination hotspots as determinants of self vs. non-self: Myths and mechanisms
Subramaniam, S., & Smith, G. R. (2022) · Advances in genetics · doi:10.1016/bs.adgen.2022.06.001 · Cited by 13
Codon pair bias deoptimization of the major oncogene meq of a very virulent Marek’s disease virus
Khedkar, P. H., Osterrieder, N., & Kunec, D. (2018) · Journal of General Virology · doi:10.1099/jgv.0.001136 · Cited by 11
A unifying network modeling approach for codon optimization
Karaşan, O. E., Şen, A., Tiryaki, B., & Çiçek, A. E. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac428 · Cited by 10
Analysis of regulation of the ilvGMEDA operon by using leader-attenuator-galK gene fusions
Lawther, R. P., Lopes, J. M., Ortuno, M. J., et al. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.5.2320-2327.1990 · Cited by 10
Attenuation of Viruses by Large-Scale Recoding of their Genomes: the Selection Is Always Biased
Osterrieder, N., & Kunec, D. (2018) · Current Clinical Microbiology Reports · doi:10.1007/s40588-018-0080-3 · Cited by 11
“Some codon pairs are found in open reading frames (ORFs) significantly more or less frequently than would be expected based on the overall frequencies of two codons that form a particular codon pair [16, 21, 44] .”
Background
Cloning, Expression, Purification and Evaluation of the Biological Properties of the Recombinant Human Growth Hormone (hGH) in Escherichia coli
Juibari, A. D., Ghovvati, S., Vaziri, H., et al. (2019) · International Journal of Peptide Research and Therapeutics · doi:10.1007/s10989-019-09854-y · Cited by 10
Peptide Linker Affecting the Activity Retention Rate of VHH in Immunosorbents
Li, D., Ren, J., Ji, F., et al. (2020) · Biomolecules · doi:10.3390/biom10121610 · Cited by 9
“Another concern is the effect of preferred codon utilization bias that may decrease the translation efficiency [28].”
Background
Reversion mutations in phosphoprotein P of a codon-pair-deoptimized human respiratory syncytial virus confer increased transcription, immunogenicity, and genetic stability without loss of attenuation
Chen, J. W., Yang, L., Santos, C. P., Hassan, S. A., Collins, P. L., Buchholz, U. J., & Nouën, C. L. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010191 · Cited by 9
“Similarly, codon-pair combinations in open reading frames (ORFs) occur more or less frequently than would be expected in a random distribution [1,2].”
Background
Codon Usage and Context Analysis of Genes Modulated during SARS-CoV-2 Infection and Dental Inflammation
Khandia, R., Pandey, M. K., Khan, A. A., Rzhepakovsky, I. V., Gurjar, P., & Karobari, M. I. (2022) · Vaccines · doi:10.3390/vaccines10111874 · Cited by 9
“There is the presence of a specific bias for a certain combinations of codons [48].”
Background
Codon choice in genes depends on flanking sequence information—implications for theoretical reverse translation
Sivaraman, K., Seshasayee, A. S. N., Tarwater, P. M., & Cole, A. M. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkm1181 · Cited by 9
“Gutman and Hatfield (6) show that there is a strong first-order Markovian relationship between codons in a gene and this relation is seen even after translation, in proteins.”
Background
iCODA: RNAi-Based Inducible Knock-In System in Trypanosoma brucei
Ringpis, G.-E. E., Lathrop, R. H., & Aphasizhev, R. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-018-8_2 · Cited by 9
A fuzzy classifier to taxonomically group DNA fragments within a metagenome
Nasser, S., Breland, A. E., Harris, F. C., & Nicolescu, M. N. (2008) · Annual Meeting of the North American Fuzzy Information Processing Society (NAFIPS) · doi:10.1109/nafips.2008.4531252 · Cited by 8
“For example a study conducted on E-coli revealed a non random utilization of codon pairs [6].”
Background
An Evolutionary Perspective of Codon Usage Pattern, Dinucleotide Composition and Codon Pair Bias in Prunus Necrotic Ringspot Virus
Wang, L., Zhao, H., Wang, Z., Ding, S., Qin, L., Jiang, R., Deng, X., He, Z. J., & Li, L. (2023) · Genes · doi:10.3390/genes14091712 · Cited by 7
Systematic analysis of the codon usage patterns of African swine fever virus genome coding sequences reveals its host adaptation phenotype
Wang, Y., Chi, C., Zhang, J., Zhang, K., Deng, D., Zheng, W., Chen, N., Meurens, F., & Zhu, J. (2024) · Microbial Genomics · doi:10.1099/mgen.0.001186 · Cited by 7
“Codon pair bias (CPB) refers to the non-random usage of synonymous codon pairs within protein-coding regions of genomes [35].”
Background
A pair of non-optimal codons are necessary for the correct biosynthesis of the Aspergillus nidulans urea transporter, UreA
Sanguinetti, M., Iriarte, A., Amillis, S., Marı́n, M., Musto, H., & Ramón, A. (2019) · Royal Society Open Science · doi:10.1098/rsos.190773 · Cited by 6
Evolutionary Patterns of Codon Usage in Major Lineages of Porcine Reproductive and Respiratory Syndrome Virus in China
Wu, W., Ge, X., Zhang, Y., Han, J., Guo, X., Zhou, L., & Yang, H. (2021) · Viruses · doi:10.3390/v13061044 · Cited by 7
“Similarly, but independently of codon bias, the juxtaposition of codons in ORFs does not appear to be randomly distributed either [32], and these preferences are typically referred to as codon pair bias.”
Background
Design of typical genes for heterologous gene expression
Simm, D., Popova, B., Braus, G. H., Waack, S., & Kollmar, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-13089-1 · Cited by 7
Regulation of Human Formyl Peptide Receptor 1 Synthesis: Role of Single Nucleotide Polymorphisms, Transcription Factors, and Inflammatory Mediators
Miettinen, H. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028712 · Cited by 7
“However, some codons are used more or less frequently, indicating a certain codon bias [5].”
Background
A Programme for Determination of Codons and Codons Context Frequency of Occurrence in Sequenced Genomes
Kirilov, K., & Ivanov, I. (2012) · Biotechnology & Biotechnological Equipment · doi:10.5504/bbeq.2012.0074 · Cited by 12
Protein yield is tunable by synonymous codon changes of translation initiation sitesPreprint
Bhandari, B. K., Lim, C. S., Remus, D. M., Chen, A., van Dolleweerd, C. J., & Gardner, P. P. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/726752 · Cited by 7
Selective constraints in yeast genes with differential expressivity: Codon pair usage and mRNA stability perspectives
Kahali, B., Ahmad, S., & Ghosh, T. C. (2011) · Gene · doi:10.1016/j.gene.2011.04.009 · Cited by 7
Dicodon-based measures for modeling gene expression
Alonso, A. M., & Diambra, L. A. (2023) · Bioinformatics · doi:10.1093/bioinformatics/btad380 · Cited by 6
Human parainfluenza virus 3 vaccine candidates attenuated by codon-pair deoptimization are immunogenic and protective in hamsters
Afroz, S., Saul, S., Dai, J., Surman, S. R., Liu, X., Park, H.-S., Nouën, C. L., Lingemann, M., Dahal, B., Coleman, J. R., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2316376121 · Cited by 6
“Certain synonymous codon pairs may be present in a species in a greater or lesser abundance than statistically predicted, a phenomenon known as codon - pair bias (CPB) (18).”
Influential
Heterologous Pathway Engineering
Niu, W., Guo, J., & Dien, S. V. (2016) · Springer eBooks · doi:10.1007/978-3-319-41966-4_3 · Cited by 6
Analysis of the use of codon pairs in the HE gene of the ISA virus shows a correlation between bias in HPR codon-pair use and mortality rates caused by the virus
Tello, M., Saavedra, J. M., & Spencer, E. (2013) · Virology Journal · doi:10.1186/1743-422x-10-180 · Cited by 5
“As with the synonymous codons, the codon pairs are distributed in the genes differently according to their level of gene expression [21].”
Background
Evaluation of GFP reporter utility for analysis of transcriptional slippage during gene expression
Wons, E., Koscielniak, D., Szadkowska, M., & Sęktas, M. (2018) · Microbial Cell Factories · doi:10.1186/s12934-018-0999-3 · Cited by 5
Two regions in human DNA polymerase β mRNA suppress translation inEscherichia coli
Date, T., Tanihara, K., Yamamoto, S., et al. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.18.4859 · Cited by 5
CCC CGA is a weak translational recoding site in Escherichia coli
Shu, P., Dai, H., Mandecki, W., & Goldman, E. (2004) · Gene · doi:10.1016/j.gene.2004.08.012 · Cited by 5
Tailoring the Immune Response via Customization of Pathogen Gene Expression
Runco, L. M., Stauft, C. B., & Coleman, J. R. (2014) · Journal of Pathogens · doi:10.1155/2014/651568 · Cited by 5
“The CPB-modulation of genes that relies on DNA synthesis and user-directed design allows for amore fine-tuned control of expression as compared to gene knockout and other conventional genetic modifications [2, 5, 6].”
BackgroundMethod
Computational tools for synthetic gene optimization
Cheema, N., Papamichail, G. P., & Papamichail, D. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-824469-2.00018-x · Cited by 6
Gene recoding by synonymous mutations creates promiscuous intragenic transcription initiation in mycobacteria
Hegelmeyer, N. K., Parkin, L. A., Previti, M. L., Andrade, J., Utama, R., Sejour, R., Gardin, J., Muller, S., Ketchum, S., Yurovsky, A., et al. (2023) · mBio · doi:10.1128/mbio.00841-23 · Cited by 4
“The idea that synonymous mutations can cause phenotypes is not new (1, 33–37).”
Background

Authors: Gutman, G. A., & Hatfield, G. W.
Affiliations: University of California, Irvine (US)
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 1989-05
Volume: 86
Issue: 10
Pages: 3699-3703
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.86.10.3699
PMC: PMC287207
OpenAlex: W2063504601
Semantic Scholar: 2e078282edbdc0cc228e53846cc1e546a9101d97
Cited by: 261
References: 38
Citations by year: 2026: 4 · 2025: 1 · 2024: 6 · 2023: 6 · 2022: 9 · 2021: 16 · 2020: 14 · 2019: 16 · 2018: 8 · 2017: 17 · 2016: 11 · 2015: 14 · 2014: 11 · 2013: 7 · 2012: 12
FWCI: 2.73
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed (publishedVersion)
PubMed Central (submittedVersion)
Funders: University of Southern California
U.S. Public Health Service
University of California, San Diego
National Institute of General Medical Sciences (GM24330)
National Institute of Allergy and Infectious Diseases (AI-21366)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords: codon pair bias, Escherichia coli, gene expression levels, translation efficiency, protein-coding sequences, codon usage
MeSH terms: Bacterial Proteins, Codon, DNA, Bacterial, Escherichia coli, Gene Expression Regulation, Genes, Bacterial, Peptide Chain Termination, Translational, Probability, RNA, Messenger

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Nonrandom utilization of codon pairs in Escherichia coli.

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