A Detailed Analysis of Codon Usages Bias and Affecting Factors in the Topoisomerase II Gene of Invertebrate iridescent virus 6

Year 2024, , 492 - 503, 27.06.2024

Yeşim Aktürk Dizman

https://doi.org/10.35414/akufemubid.1388197

Abstract

The topoisomerase II protein (ORF 045L) of invertebrate iridescent virus 6 (IIV6) plays essential roles in managing DNA topology during viral replication and transcription. Considering the importance of the topoisomerase II gene, a comprehensive analysis was conducted to explore the codon usage bias (CUB) of topoisomerase II genes of IIV6 and 9 reference invertebrate iridescent viruses (IIVs). In this research, the findings from the base composition analysis revealed that the IIV6 topoisomerase gene had a high A/T content, with nucleotide A being the most prevalent. The relative synonymous codon usage values for each codon demonstrated the presence of CUB. The effective number of codons (ENC) value for the IIV6 topoisomerase II gene is 34.80, signifying a significant CUB. The ENC plot indicates that all the diverse sequences lie beneath the standard curve, signifying that CUB is influenced not only by mutational pressure but also by other factors, including natural selection. The findings from the neutrality analysis indicate that the codon usage pattern (CUP) is more significantly shaped by natural selection, as evidenced by a regression line slope of 0.1602, compared to the influence of mutation pressure. Furthermore, it has been established that the nucleotide composition and dinucleotide content influence the CUB of the topoisomerase II gene in IIV6. The initial comprehensive analysis of CUB in the IIV6 topoisomerase II gene offers valuable insights into the gene's evolutionary processes.

Keywords

Invertebrate iridescent virus 6, Topoisomerase II gene, 045L, Codon usage bias

Invertebrate iridescent virüs 6’nın Topoizomeraz II Genindeki Kodon Kullanım Eğiliminin ve Etkileyen Faktörlerin Ayrıntılı Analizi

Abstract

Invertebrate iridescent virüs 6 (IIV6)’nın topoizomeraz II proteini (ORF 045L), viral replikasyon ve transkripsiyon sırasında DNA topolojisinin belirlenmesinde önemli roller oynar. Topoizomeraz II geninin önemi göz önünde bulundurularak, IIV6 ve 9 referans invertebrate iridescent virüs (IIVs)’ün topoizomeraz II genlerinin kodon kullanım eğilimini (CUB) araştırmak için kapsamlı bir analiz yapılmıştır. Bu araştırmada, baz bileşimi analizinden elde edilen bulgular, IIV6 topoizomeraz geninin yüksek bir A/T içeriğine sahip olduğunu ve A nükleotidinin en yaygın olduğunu göstermiştir. Her bir kodon için göreli sinonim kodon kullanım değerleri, kodon kullanım eğiliminin varlığını göstermiştir. IIV6 topoizomeraz II geni için etkin kodon sayısı (ENC) değeri 34,80'dir ve bu da önemli bir CUB’ye işaret etmektedir. ENC grafiği, tüm farklı dizilerin standart eğrinin altında yer aldığını ve kodon kullanım eğiliminin sadece mutasyon baskısından değil, doğal seçilim de dahil olmak üzere diğer faktörlerden de etkilendiğini göstermektedir. Nötraliti analizinden elde edilen bulgular, mutasyon baskısının etkisine kıyasla, 0,1602'lik regresyon çizgisi eğiminin de gösterdiği gibi, kodon kullanım modelinin doğal seçilim tarafından daha belirgin bir şekilde şekillendirildiğini göstermektedir. Ayrıca, nükleotid bileşiminin ve dinükleotid içeriğinin IIV6 topoizomeraz II geninin kodon kullanım eğilimini etkilediği tespit edilmiştir. IIV6 topoizomeraz II genindeki kodon kullanım eğiliminin ilk kapsamlı analizi, genin evrimsel süreçleri hakkında değerli bilgiler sunmaktadır.

Keywords

Invertebrate iridescent virus 6;, Topoisomerase II gene;, 045L;, Codon usage bias

References

• Afonso, C.L., Tulman, E.R., Delhon, G., Lu, Z., Viljoen, G.J., Wallace, D.B., Kutish, G.F. and Rock, D.L., 2006. Genome of Crocodilepox Virus. Journal of Virology, 80, 4978–4991. https://doi.org/10.1128/jvi.80.10.4978-4991.2006
• Afowowe, T.O., Sakurai, Y., Urata, S., Zadeh, V.R. and Yasuda, J., 2022. Topoisomerase II as a Novel Antiviral Target against Panarenaviral Diseases. Viruses, 15, 105. https://doi.org/10.3390/v15010105
• Aktürk Dizman, Y., 2023. Codon usage bias analysis of the gene encoding NAD+-dependent DNA ligase protein of Invertebrate iridescent virus 6. Archives of Microbiology, 205, 352. https://doi.org/10.1007/s00203-023-03688-5
• Begum, N. and Chakraborty, S., 2022. Influencing elements of codon usage bias in Birnaviridae and its evolutionary analysis. Virus Research, 310, 198672. https://doi.org/10.1016/j.virusres.2021.198672
• Berger, J.M., 1998. Structure of DNA topoisomerases. Biochimica et Biophysica Acta, 1400, 3–18. https://doi.org/10.1016/S0167-4781(98)00124-9
• Carbone, A., Zinovyev, A. and Képès, F., 2003. Codon adaptation index as a measure of dominating codon bias. Bioinformatics, 19, 2005–2015. https://doi.org/10.1093/bioinformatics/btg272
• Champoux, J.J., 2001. DNA topoisomerases: structure, function, and mechanism. Annual Review of Biochemistry, 70, 369–413. https://doi.org/10.1146/annurev.biochem.70.1.36
• Chen, Y., 2013. A comparison of synonymous codon usage bias patterns in DNA and RNA virus genomes: Quantifying the relative importance of mutational pressure and natural selection. BioMed Research International, 2013, 406342. https://doi.org/10.1155/2013/406342
• Chinchar, V.G., Waltzek, T.B. and Subramaniam, K., 2017. Ranaviruses and other members of the family Iridoviridae: Their place in the virosphere. Virology, 511, 259–271. https://doi.org/10.1016/j.virol.2017.06.007
• Coelho, J. and Leitão, A., 2020. The African swine fever virus (ASFV) topoisomerase ii as a target for viral prevention and control. Vaccines, 8, 1–16. https://doi.org/10.3390/vaccines8020312
• Comeron, J.M. and Aguadé, M., 1998. An evaluation of measures of synonymous codon usage bias. Journal of Molecular Evolution, 47, 268–274. https://doi.org/10.1007/PL00006384
• Deb, B., Uddin, A. and Chakraborty, S., 2021. Composition, codon usage pattern, protein properties, and influencing factors in the genomes of members of the family Anelloviridae. Archives of Virology, 166, 461–474. https://doi.org/10.1007/s00705-020-04890-2
• Duan, H., Zhang, Q., Wang, C., Li, F., Tian, F., Lu, Y., Hu, Y., Yang, H. and Cui, G., 2021. Analysis of codon usage patterns of the chloroplast genome in Delphinium grandiflorum L. reveals a preference for AT-ending codons as a result of major selection constraints. PeerJ, 9, e10787. https://doi.org/10.7717/peerj.10787
• Eaton, H.E., Metcalf, J., Penny, E., Tcherepanov, V., Upton, C. and Brunetti, C.R., 2007. Comparative genomic analysis of the family Iridoviridae: Re-annotating and defining the core set of iridovirus genes. Virology Journal, 4, 11. https://doi.org/10.1186/1743-422X-4-11
• Ebert, S.N., Shtrom, S.S. and Muller, M.T., 1990. Topoisomerase II cleavage of herpes simplex virus type 1 DNA in vivo is replication dependent. Journal of Virology, 64, 4059–4066. https://doi.org/10.1128/jvi.64.9.4059-4066.1990
• Fortune, J.M., Lavrukhin, O. V., Gurnon, J.R., Van Etten, J.L., Lloyd, R.S. and Osheroff, N., 2001. Topoisomerase II from Chlorella Virus PBCV-1 Has an Exceptionally High DNA Cleavage Activity. Journal of Biological Chemistry, 276, 24401–24408. https://doi.org/10.1074/jbc.M101693200
• Hartl, D.L., Moriyama, E.N. and Sawyer, S.A., 1994. Selection intensity for codon bias. Genetics, 138, 227–234. https://doi.org/10.1093/genetics/138.1.227
• He, Z., Gan, H. and Liang, X., 2019. Analysis of synonymous codon usage bias in potato virus M and its adaption to hosts. Viruses, 11, 752. https://doi.org/10.3390/v11080752
• Hernandez, O., Maldonado, G. and Williams, T., 2000. An Epizootic of Patient Iridescent Virus Disease in Multiple Species of Blackflies in Chiapas, Mexico. Medical and Veterinary Entomology, 14, 458-462. https://doi.org/10.1046/j.1365-2915.2000.00258.x
• Iriarte, A., Lamolle, G. and Musto, H., 2021. Codon Usage Bias: An Endless Tale. Journal of Molecular Evolution, 89, 589–593. https://doi.org/10.1007/s00239-021-10027-z
• Jakob, N.J. and Darai, G., 2002. Molecular anatomy of Chilo iridescent virus genome and the evolution of viral genes. Virus Genes, 25, 299-316. https://doi.org/10.1023/A:1020984210358
• Jenkins, G.M. and Holmes, E.C., 2003. The extent of codon usage bias in human RNA viruses and its evolutionary origin. Virus Research, 92, 1–7. https://doi.org/10.1016/S0168-1702(02)00309-X
• Jiang, L., Zhang, Q., Xiao, S. and Si, F., 2022. Deep decoding of codon usage strategies and host adaption preferences of soybean mosaic virus. International Journal of Biological Macromolecules, 222, 803-817. https://doi.org/10.1016/j.ijbiomac.2022.09.179
• Kariin, S. and Burge, C., 1995. Dinucleotide relative abundance extremes: a genomic signature. Trends in Genetics, 11, 283–290. https://doi.org/10.1016/S0168-9525(00)89076-9
• Khandia, R., Khan, A.A., Karuvantevida, N., Gurjar, P., Rzhepakovsky, I.V. and Legaz, I., 2023. Insights into Synonymous Codon Usage Bias in Hepatitis C Virus and Its Adaptation to Hosts. Pathogens, 12, 325. https://doi.org/10.3390/pathogens12020325
• Kleespies, R.G., Tidona, C.A. and Darai, G., 1999. Characterization of a New Iridovirus Isolated from Crickets and Investigations on the Host Range. Journal of Invertebrate Pathology, 73, 84-90. https://doi.org/10.1006/jipa.1998.4821
• Kumar, N., Bera, B.C., Greenbaum, B.D., Bhatia, S., Sood, R., Selvaraj, P., Anand, T., Tripathi, B.N. and Virmani, N., 2016. Revelation of influencing factors in overall codon usage bias of equine influenza viruses. PLoS One 11, 1–26. https://doi.org/10.1371/journal.pone.0154376
• Kumar, N., Kulkarni, D.D., Lee, B., Kaushik, R., Bhatia, S., Sood, R., Pateriya, A.K., Bhat, S. and Singh, V.P., 2018. Evolution of codon usage bias in henipaviruses is governed by natural selection and is host-specific. Viruses, 10, 604. https://doi.org/10.3390/v10110604
• Liu, X., 2013. A more accurate relationship between “effective number of codons” and GC3s under assumptions of no selection. Computational Biology and Chemistry, 42, 35–39. https://doi.org/10.1016/j.compbiolchem.2012.11.003
• Machado, H.E., Lawrie, D.S. and Petrov, D.A., 2020. Pervasive Strong Selection at the Level of Codon Usage Bias in Drosophila melanogaster. Genetics, 214, 511–528. https://doi.org/10.1534/genetics.119.302542
• Molteni, C., Forni, D., Cagliani, R., Bravo, I.G. and Sironi, M., 2023. Evolution and diversity of nucleotide and dinucleotide composition in poxviruses. Journal of General Virology, 104, 1–19. https://doi.org/10.1099/jgv.0.001897
• Nasrullah, I., Butt, A.M., Tahir, S., Idrees, M. and Tong, Y., 2015. Genomic analysis of codon usage shows influence of mutation pressure, natural selection, and host features on Marburg virus evolution. BMC Evolutionary Biology, 15, 1–15. https://doi.org/10.1186/s12862-015-0456-4
• Nyayanit, D.A., Yadav, P.D., Kharde, R. and Cherian, S., 2021. Natural selection plays an important role in shaping the codon usage of structural genes of the viruses belonging to the coronaviridae family. Viruses, 13, 3. https://doi.org/10.3390/v13010003
• Odon, V., Fros, J.J., Goonawardane, N., Dietrich, I., Ibrahim, A., Alshaikhahmed, K., Nguyen, D. and Simmonds, P., 2019. The role of ZAP and OAS3/RNAseL pathways in the attenuation of an RNA virus with elevated frequencies of CpG and UpA dinucleotides. Nucleic Acids Research, 47, 8061–8083. https://doi.org/10.1093/nar/gkz581
• Ouyang, T., Zhong, J., Chai, Z., Wang, J., Zhang, M., Wu, Z. and Xin, J., 2022. Codon Usage Bias and Cluster Analysis of the MMP-2 and MMP-9 Genes in Seven Mammals. Genetics Research, 2022, 2823356. https://doi.org/10.1155/2022/2823356
• Parvathy, S.T., Udayasuriyan, V. and Bhadana, V., 2022. Codon usage bias. Molecular Biology Reports, 49, 539–565. https://doi.org/10.1007/s11033-021-06749-4
• Patil, S.S., Indrabalan, U.B., Suresh, K.P. and Shome, B.R., 2021. Analysis of codon usage bias of classical swine fever virus. Veterinary World, 14, 1450–1458. https://doi.org/10.14202/vetworld.2021.1450-1458
• Puigbò, P., Bravo, I.G. and Garcia-Vallve, S., 2008. CAIcal: A combined set of tools to assess codon usage adaptation. Biology Direct, 3, 38. https://doi.org/10.1186/1745-6150-3-38
• Shackelton, L.A., Parrish, C.R. and Holmes, E.C., 2006. Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. Journal of Molecular Evolution, 62, 551–563. https://doi.org/10.1007/s00239-005-0221-1
• Sharma, A., Gupta, S. and Paul, K., 2023. Codon usage behavior distinguishes pathogenic Clostridium species from the non-pathogenic species. Gene, 873, 147394. https://doi.org/10.1016/j.gene.2023.147394
• Sharp, C., Thompson, B., Nash, T., Diebold, O., Pinto, R., Thorley, L., Lin, Y., Sives, S., Wise, H., Clohisey Hendry, S., Grey, F., Vervelde, L., Simmonds, P., Digard, P. and Gaunt, E., 2023. CpG dinucleotide enrichment in the influenza A virus genome as a live attenuated vaccine development strategy. PLoS Pathogens, 19, e1011357. https://doi.org/10.1371/journal.ppat.1011357
• Sharp, P.M. and Li, W.H., 1986. An evolutionary perspective on synonymous codon usage in unicellular organisms. Journal of Molecular Evolution, 24, 28–38. https://doi.org/10.1007/BF02099948
• Shi, S.L., Jiang, Y.R., Yang, R.S., Wang, Y. and Qin, L., 2016. Codon usage in Alphabaculovirus and Betabaculovirus hosted by the same insect species is weak, selection dominated and exhibits no more similar patterns than expected. Infection, Genetics and Evolution, 44, 412–417. https://doi.org/10.1016/j.meegid.2016.07.042
• Si, F., Jiang, L., Yu, R., Wei, W. and Li, Z., 2021. Study on the Characteristic Codon Usage Pattern in Porcine Epidemic Diarrhea Virus Genomes and Its Host Adaptation Phenotype. Frontiers in Microbiology, 12, 1–18. https://doi.org/10.3389/fmicb.2021.738082
• Spencer, P.S. and Barral, J.M., 2012. Genetic code redundancy and its influence on the encoded polypeptides. Computational and Structural Biotechnology Journal, 1, e201204006. https://doi.org/10.5936/csbj.201204006
• Sueoka, N., 1988. Directional mutation pressure and neutral molecular evolution. Proceedings of the National Academy of Sciences of the United States of America, 85, 2653–2657. https://doi.org/10.1073/pnas.85.8.2653
• Suzuki, H., Brown, C.J., Forney, L.J. and Top, E.M., 2008. Comparison of correspondence analysis methods for synonymous codon usage in bacteria. DNA Research, 15, 357–365. https://doi.org/10.1093/dnares/dsn028
• Tamura, K., Stecher, G. and Kumar, S., 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38, 3022–3027. https://doi.org/10.1093/molbev/msab120
• Tao, P., Dai, L., Luo, M., Tang, F., Tien, P. and Pan, Z., 2009. Analysis of synonymous codon usage in classical swine fever virus. Virus Genes, 38, 104–112. https://doi.org/10.1007/s11262-008-0296-z
• Tian, H. feng, Hu, Q. mu, Xiao, H. bing, Zeng, L. bing, Meng, Y. and Li, Z., 2020. Genetic and codon usage bias analyses of major capsid protein gene in Ranavirus. Infection, Genetics and Evolution, 84, 104379. https://doi.org/10.1016/j.meegid.2020.104379
• Wei, L., He, J., Jia, X., Qi, Q., Liang, Z., Zheng, H., Ping, Y., Liu, S. and Sun, J., 2014. Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution. BMC Evolutionary Biology, 14, 1–12. https://doi.org/10.1186/s12862-014-0262-4
• Wright, F., 1990. The “effective number of codons” used in a gene. Gene, 87, 23–29. https://doi.org/10.1016/0378-1119(90)90491-9
• Wu, H., Bao, Z., Mou, C., Chen, Z. and Zhao, J., 2020. Comprehensive Analysis of Codon Usage on Porcine Astrovirus. Viruses, 12, 991. https://doi.org/10.3390/v12090991
• Xu, X., Fei, D., Han, H., Liu, H., Zhang, J. Zhou, Y., Xu, C., Wang, H., Cao, H. and Zhang, H., 2017. Comparative characterization analysis of synonymous codon usage bias in classical swine fever virus. Microbial Pathogenesis, 107, 368–371. https://doi.org/10.1016/j.micpath.2017.04.019
• Yan, X., Yu, Z., Zhang, P., Battisti, A.J., Holdaway, H.A., Chipman, P.R., Bajaj, C., Bergoin, M., Rossmann, M.G. and Baker, T.S., 2009. The Capsid Proteins of a Large, Icosahedral dsDNA Virus. Journal of Molecular Biology, 385, 1287–1299. https://doi.org/10.1016/j.jmb.2008.11.002
• Yu, X., Gao, K., Pi, M., Li, H., Zhong, W., Li, B. and Ning, Z., 2021. Phylogenetic and codon usage analysis for replicase and capsid genes of porcine circovirus 3. Veterinary Research Communications, 45, 353-361. https://doi.org/10.1007/s11259-021-09816-0
• Zhang, X., Cai, Y., Zhai, X., Liu, J., Zhao, W., Ji, S., Su, S. and Zhou, J., 2018. Comprehensive analysis of codon usage on rabies virus and other lyssaviruses. International Journal of Molecular Sciences, 19, 2397. https://doi.org/10.3390/ijms19082397
• Zhao, R., Gu, C., Zou, X., Zhao, M., Xiao, W., He, M., He, L., Yang, Q., Geng, Y. and Yu, Z., 2022. Comparative genomic analysis reveals new evidence of genus boundary for family Iridoviridae and explores qualified hallmark genes. Computational and Structural Biotechnology Journal, 20, 3493–3502. https://doi.org/10.1016/j.csbj.2022.06.049
• Zhou, J., Gao, Z., Zhang, J., Ding, Y., Stipkovits, L., Szathma, S., Pejsak, Z. and Liu, Y., 2013. The analysis of codon bias of foot-and-mouth disease virus and the adaptation of this virus to the hosts. Infection, Genetics and Evolution, 14, 105–110. https://doi.org/10.1016/j.meegid.2012.09.02
• National Center for Biotechnology Information, http://www.ncbi.nlm.nih.gov, (1.10.2023)
• CodonW,http://codonw.sourceforge.net/, (16.10.2023)
• CAIcal server, http://genomes.urv.es/CAIcal/, (17.10.2023)
• https://www.bioinformatics.nl/cgi-bin/emboss/ compseq, (23.10.2023)
• RCDI server, http://genomes.urv.cat/CAIcal/RCDI/, (17.10.2023)
• Codon and Codon Pair Usage Tables, https://dnahive.fda.gov/dna.cgi?cmd=codon_usage &id=537&mode=cocoputs, (15.10.2023)