A Comprehensive Comparative Analysis on the Codon Usage Bias of DNA Polymerase Genes in Invertebrate Iridescent Viruses

Yıl 2024, , 32 - 48, 30.06.2024

Yeşim Aktürk Dizman

https://doi.org/10.53501/rteufemud.1416072

Öz

Invertebrate iridescent viruses (IIVs) are classified as double-stranded DNA viruses within the Iridoviridae family. IIVs are viruses that infect invertebrate hosts, causing symptoms that vary in intensity from slight reductions in host fitness to systemic disease. Numerous earlier investigations have provided insights into the genomic, proteomic, and transcriptional analyses of invertebrate iridescent viruses. However, the codon usage bias (CUB) of IIVs has yet to be fully understood. In order to gain a more profound insight into the evolutionary features of IIVs, we conducted an extensive analysis of the codon usage patterns in the DNA polymerase genes (DNA pol genes) of 12 invertebrate iridescent viruses. The analysis of both nucleotide composition and relative synonymous codon usage (RSCU) indicated a higher prevalence of AT-ended codons in the DNA pol genes of IIVs. Additionally, a low codon usage bias was determined from the effective number of codons (ENC) value. Analyses of ENC-GC3s plot, neutrality plot, and parity rule 2 plot illustrated that the codon usage patterns in IIVs DNA pol genes were influenced by both natural selection and mutational pressure. This investigation holds significance as it has delineated the codon usage patterns within the DNA pol genes of IIVs and has furnished crucial data for a foundational study of their evolutionary aspects.

Anahtar Kelimeler

DNA polymerase, Invertebrate iridescent viruses, Codon usage bias, Mutation pressure, Natural selection

Invertebrate Iridescent Virüslerdeki DNA Polimeraz Genlerinin Kodon Kullanım Eğilimi Üzerine Ayrıntılı Karşılaştırmalı Bir Analiz

Öz

Invertebrate iridescent virüsler (IIV’ler), Iridoviridae familyası içerinde yer alan çift sarmallı DNA virüsleri olarak sınıflandırılır. IIV’ler omurgasız konakçıları enfekte eden, konak hareketinde hafif azalmalardan sistemik hastalığa kadar değişen yoğunlukta semptomlara neden olan virüslerdir. Daha önce yapılan çok sayıda araştırma, invertebrate iridescent virüslerin genomik, proteomik ve transkripsiyonel analizlerine ilişkin bilgiler sağlamıştır. Bununla birlikte, IIV'lerin kodon kullanım eğilimi henüz tam olarak anlaşılamamıştır. IIV'lerin evrimsel özellikleri hakkında daha derin bir bilgi elde etmek için, 12 invertebrate iridescent virüsün DNA polimeraz genlerindeki kodon kullanım modellerinin kapsamlı bir analizini gerçekleştirdik. Hem nükleotid kompozisyonu hem de göreli sinonim kodon kullanımı (RSCU) analizi, IIV'lerin DNA pol genlerinde AT-uçlu kodonların daha yüksek bir yaygınlıkta bulunduğunu göstermiştir. Ayrıca, etkin kodon sayısı (ENC) değerinden düşük bir kodon kullanım yanlılığı tespit edilmiştir. ENC-GC3s grafiği, nötraliti grafiği ve parite kuralı 2 grafiği analizleri, IIV’lerin DNA pol genlerindeki kodon kullanım modellerinin hem doğal seçilim hem de mutasyon baskısından etkilendiğini göstermiştir. Bu araştırma, IIV'lerin DNA pol genlerindeki kodon kullanım modellerini tanımlaması ve evrimsel yönlerine ilişkin temel bir çalışma için önemli veriler sağlaması açısından önem taşımaktadır.

Anahtar Kelimeler

DNA polimeraz, Invertebrate iridescent virüsler, Kodon kullanım eğilimi, Mutasyon baskısı, Doğal seçilim

Kaynakça

• 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(11), 1–19. https://doi.org/10.1007/s00203-023-03688-5
• Andargie, M., Congyi, Z. (2022). Genome-wide analysis of codon usage in sesame (Sesamum indicum L.). Heliyon, 8(1), e08687. https://doi.org/10.1016/j.heliyon.2021.e08687
• Ata, G., Wang, H., Bai, H., Yao, X., Tao, S. (2021). Edging on mutational bias, induced natural selection from host and natural reservoirs predominates codon usage evolution in hantaan virus. Frontiers in Microbiology, 12, 1–18. https://doi.org/10.3389/fmicb.2021.699788
• Bassetto, M., Van Dycke, J., Neyts, J., Brancale, A., Rocha-Pereira, J. (2019). Targeting the viral polymerase of diarrhea-causing viruses as a strategy to develop a single broad-spectrum antiviral therapy. Viruses, 11(2), 173. https://doi.org/10.3390/v11020173
• Behura, S.K., Severson, D.W. (2013). Codon usage bias: Causative factors, quantification methods and genome-wide patterns: With emphasis on insect genomes. Biological Reviews, 88(1), 49–61. https://doi.org/10.1111/j.1469-185X.2012.00242.x
• Bera, B.C., Virmani, N., Kumar, N., Anand, T., Pavulraj, S., Rash, A., Elton, D., Rash, N., Bhatia, S., Sood, R., Singh, R.K., Tripathi, B.N. (2017). Genetic and codon usage bias analyses of polymerase genes of equine influenza virus and its relation to evolution. BMC Genomics, 18(1), 652. https://doi.org/10.1186/s12864-017-4063-1
• Biswas, K.K., Palchoudhury, S., Chakraborty, P., Bhattacharyya, U.K., Ghosh, D.K., Debnath, P., Ramadugu, C., Keremane, M.L., Khetarpal, R.K., Lee, R.F. (2019). Codon usage bias analysis of Citrus tristeza virus: Higher codon adaptation to Citrus reticulata host. Viruses, 11(4), 1–17. https://doi.org/10.3390/v11040331
• Canuti, M., Large, G., Verhoeven, J.T.P., Dufour, S.C. (2022). A novel iridovirus discovered in deep-sea carnivorous sponges. Viruses, 14(8), 1595. https://doi.org/10.3390/v14081595
• Carbone, A., Zinovyev, A., Képès, F. (2003). Codon adaptation index as a measure of dominating codon bias. Bioinformatics, 19(16), 2005–2015. https://doi.org/10.1093/bioinformatics/btg272
• Chakraborty, S., Yengkhom, S., Uddin, A. (2020). Analysis of codon usage bias of chloroplast genes in Oryza species: Codon usage of chloroplast genes in Oryza species. Planta, 252(4), 1–20. https://doi.org/10.1007/s00425-020-03470-7
• Chen, G., Fang, Y., Yan, Q., Li, P., Wu, L., Feng, G. (2019). The deficiency in nuclear localization signal of Neodiprion lecontei nucleopolyhedrovirus DNA polymerase prevents rescue of viral DNA replication and virus production in DNApol-null Autographa californica multiple nucleopolyhedrovirus. Virus Research, 266, 52–57. https://doi.org/https://doi.org/10.1016/j.virusres.2019.04.005
• Chen, L., Liu, T., Yang, D., Nong, X., Xie, Y., Fu, Y., Wu, X., Huang, X., Gu, X., Wang, S., Peng, X., Yang, G. (2013). Analysis of codon usage patterns in Taenia pisiformis through annotated transcriptome data. Biochemical and Biophysical Research Communications, 430(4), 1344–1348. https://doi.org/10.1016/j.bbrc.2012.12.078
• Chen, Y., Xu, Q., Tan, C., Li, X., Chi, X., Cai, B., Yu, Z., Ma, Y., Chen, J.L. (2017). Genomic analysis of codon usage shows influence of mutation pressure, natural selection, and host features on Senecavirus A evolution. Microbial Pathogenesis, 112, 313–319. https://doi.org/10.1016/j.micpath.2017.09.040
• Cho, M., Kim, H., Son, H.S. (2019). Codon usage patterns of LT-AG genes in polyomaviruses from different host species. Virology Journal, 16(1), 1–24. https://doi.org/10.1186/s12985-019-1245-2
• Coen, D.M., Lawler, J.L., Abraham, J. (2021). Herpesvirus DNA polymerase: Structures, functions, and mechanisms. Enzymes, 50, 133–178. https://doi.org/https://doi.org/10.1016/bs.enz.2021.09.003
• Delhon, G., Tulman, E.R., Afonso, C.L., Lu, Z., Becnel, J.J., Moser, B.A., Kutish, G.F., Rock, D.L. (2006). Genome of invertebrate iridescent virus type 3 (mosquito iridescent virus). Journal of Virology, 80(17), 8439–8449. https://doi.org/10.1128/jvi.00464-06
• Dizman, Y.A., Muratoglu, H., Sandalli, C., Nalcacioglu, R., Demirbag, Z. (2016). Chilo iridescent virus (CIV) ORF 012L encodes a protein with both exonuclease and endonuclease functions. Archives of Virology, 161(11), 3029–3037. https://doi.org/10.1007/s00705-016-3007-4
• Eaton, H.E., Metcalf, J., Penny, E., Tcherepanov, V., Upton, C., 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
• Eaton, H.E., Ring, B.A., Brunetti, C.R. (2010). The genomic diversity and phylogenetic relationship in the family Iridoviridae. Viruses, 2(7), 1458–1475. https://doi.org/10.3390/v2071458
• Feng, H., Segalés, J., Wang, F., Jin, Q., Wang, A., Zhang, G., Franzo, G. (2022). Comprehensive analysis of codon usage patterns in chinese porcine circoviruses based on their major protein-coding sequences. Viruses. 14, 81. https://doi.org/10.3390/v14010081
• Fu, Y., Liang, F., Li, C., Warren, A., Shin, M.K., Li, L. (2023). Codon usage bias analysis in macronuclear genomes of ciliated protozoa. Microorganisms, 11(7), 1833. https://doi.org/10.3390/microorganisms11071833
• Garro, H.A., Pungitore, C.R. (2019). DNA related enzymes as molecular targets for antiviral and antitumoral chemotherapy. a natural overview of the current perspectives. Current Drug Targets, 20(1), 70–80. https://doi.org/10.2174/1389450119666180426103558
• He, W., Wang, N., Tan, J., Wang, R., Yang, Y., Li, G., Guan, H., Zheng, Y., Shi, X., Ye, R., Su, S., Zhou, J. (2019). Comprehensive codon usage analysis of porcine deltacoronavirus. Molecular Phylogenetics and Evolution. 141, 106618. https://doi.org/10.1016/j.ympev.2019.106618
• Hu, Z., Kuritzkes, D.R. (2014). Altered viral fitness and drug susceptibility in HIV-1 carrying mutations that confer resistance to nonnucleoside reverse transcriptase and integrase strand transfer inhibitors. Journal of Virology, 88(16):9268-76. https://doi.org/10.1128/jvi.00695-14
• İnce, İ.A., Özcan, O., Ilter-Akulke, A.Z., Scully, E.D., Özgen, A. (2018). Invertebrate iridoviruses: A glance over the last decade. Viruses, 10(4), 1–25. https://doi.org/10.3390/v10040161
• Iriarte, A., Lamolle, G., Musto, H. (2021). Codon usage bias: An endless tale. Journal of Molecular Evolution, 89(9-10), 589–593. https://doi.org/10.1007/s00239-021-10027-z
• Jakob, N.J., Darai, G. (2002). Molecular anatomy of Chilo iridescent virus genome and the evolution of viral genes. Virus Genes, 25(3), 299–316. https://doi.org/10.1023/A:1020984210358
• Jakob, N.J., Müller, K., Bahr, U., Darai, G. (2001). Analysis of the first complete DNA sequence of an invertebrate iridovirus: Coding strategy of the genome of Chilo iridescent virus. Virology, 286(1), 182–196. https://doi.org/10.1006/viro.2001.0963
• Karumathil, S., Raveendran, N.T., Ganesh, D., Kumar NS, S., Nair, R.R., Dirisala, V.R. (2018). Evolution of synonymous codon usage bias in west african and central african strains of monkeypox virus. Evolutionary Bioinformatics, 14. https://doi.org/10.1177/1176934318761368
• Khandia, R., Singhal, S., Kumar, U., Ansari, A., Tiwari, R., Dhama, K., Das, J., Munjal, A.O., Singh, R.K. (2019). Analysis of nipah virus codon usage and adaptation to hosts. Frontiers in Microbiology, 10, 1–18. https://doi.org/10.3389/fmicb.2019.00886
• Komar, A.A. (2016). The Yin and Yang of codon usage. Human Molecular Genetics, 25, 77–85. https://doi.org/https://doi.org/10.1093/hmg/ddw207
• Li, G., Zhang, L., Xue, P. (2022). Codon usage divergence of important functional genes in Mycobacterium tuberculosis. International Journal of Biological Macromolecules, 209(2), 1197–1204. https://doi.org/10.1016/j.ijbiomac.2022.04.112
• Lu, M., Wan, W., Li, Y., Li, H., Sun, B., Yu, K., Zhao, J., Franzo, G., Su, S. (2023). Codon usage bias analysis of the spike protein of human coronavirus 229E and its host adaptability. International Journal of Biological Macromolecules, 253, 127319. https://doi.org/10.1016/j.ijbiomac.2023.127319
• Mesplède, T., Quashie, P.K., Osman, N., Han, Y., Singhroy, D.N., Lie, Y., Petropoulos, C.J., Huang, W., Wainberg, M.A. (2013). Viral fitness cost prevents HIV-1 from evading dolutegravir drug pressure. Retrovirology, 22(10), 22. https://doi.org/10.1186/1742-4690-10-22
• Nalçacioǧlu, R., Ince, I.A., Vlak, J.M., Demirbaǧ, Z., van Oers, M.M. (2007). The Chilo iridescent virus DNA polymerase promoter contains an essential AAAAT motif. Journal of General Virology, 88(9), 2488–2494. https://doi.org/10.1099/vir.0.82947-0
• Nalçacioǧlu, R., Marks, H., Vlak, J.M., Demirbaĝ, Z., Van Oers, M.M. (2003). Promoter analysis of the Chilo iridescent virus DNA polymerase and major capsid protein genes. Virology, 317(2), 321–329. https://doi.org/10.1016/j.virol.2003.08.007
• Nambou, K., Anakpa, M. (2020). Deciphering the co-adaptation of codon usage between respiratory coronaviruses and their human host uncovers candidate therapeutics for COVID-19. Infection, Genetics and Evolution. 85, 104471. https://doi.org/10.1016/j.meegid.2020.104471
• Nguyen, T.H., Wang, D., Rahman, S.U., Bai, H., Yao, X., Chen, D., Tao, S. (2021). Analysis of codon usage patterns and influencing factors in rice tungro bacilliform virus. Infection, Genetics and Evolution, 90. https://doi.org/10.1016/j.meegid.2021.104750
• Noor, F., Ashfaq, U.A., Bakar, A., Qasim, M., Masoud, M.S., Alshammari, A., Alharbi, M., Riaz, M.S. (2023). Identification and characterization of codon usage pattern and influencing factors in HFRS-causing hantaviruses. Frontiers in Immunology. 14, 1131647. https://doi.org/10.3389/fimmu.2023.1131647
• Palanisamy, N., Osman, N., Ohnona, F., Xu, H.T., Brenner, B., Mesplède, T., Wainberg, M.A. (2017). Does antiretroviral treatment change HIV-1 codon usage patterns in its genes: a preliminary bioinformatics study, AIDS Research and Therapy, 14(1), 2. https://doi.org/10.1186/s12981-016-0130-y
• Prabha, R., Singh, D.P., Gupta, S.K., Farooqi, S., Rai, A. (2012). Synonymous codon usage in Thermosynechococcus elongatus (cyanobacteria) identifies the factors shaping codon usage variation. Bioinformation, 8(13), 622–628. https://doi.org/10.6026/97320630008622
• Puigbò, P., Bravo, I.G., 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
• Rahman, S.U., Rehman, H.U., Rahman, I.U., Rauf, A., Alshammari, A., Alharbi, M., Haq, N.U., Suleria, H.A.R., Raza, S.H.A. (2022). Analysis of codon usage bias of lumpy skin disease virus causing livestock infection. Frontiers in Veterinary Science, 9, 1071097. https://doi.org/10.3389/fvets.2022.1071097
• Rani, S., Mamathashree, M.N., Bharthi, I.U., Patil, S.S., Krishnamoorthy, P., Shueb, M., Pandey, R.K., Suresh, K.P. (2023). Comprehensive examination on codon usage bias pattern of the Bovine Ephemeral fever virus. Journal of Biomolecular Structure and Dynamics. 1, 11. https://doi.org/10.1080/07391102.2023.2258220
• Rao, Y., Wang, Z., Chai, X., Nie, Q., Zhang, X. (2014). Hydrophobicity and aromaticity are primary factors shaping variation in amino acid usage of chicken proteome. PLoS One, 9(10), 1–10. https://doi.org/10.1371/journal.pone.0110381
• Schnitzler, P., Soltau, J.B., Fischer, M., Reisner, H., Scholz, J., Delius, H., Darai, G. (1987). Molecular cloning and physical mapping of the genome of insect iridescent virus type 6: Further evidence for circular permutation of the viral genome. Virology, 160(1), 66–74. https://doi.org/10.1016/0042-6822(87)90045-6
• Sharp, P.M., Li, W.H. (1987). The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research, 15(3), 1281–1295. https://doi.org/10.1093/nar/15.3.1281
• Sharp, P.M., Li, W.H. (1986). An evolutionary perspective on synonymous codon usage in unicellular organisms. Journal of Molecular Evolution, 24(19), 28–38. https://doi.org/10.1007/BF02099948
• Sharp, P.M., Stenico, M., Peden, J.F., Lloyd, A.T. (1993). Codon usage: mutational bias, translational selection, or both? Biochemical Society Transactions, 21(4), 835–841. https://doi.org/10.1042/bst0210835
• Smith, R.D. (2022). Enhanced effective codon numbers to understand codon usage bias. Biosystems, 220. https://doi.org/https://doi.org/10.1016/j.biosystems.2022.104734
• Sueoka, N. (1999). Two aspects of DNA base composition: G+C content and translation- coupled deviation from intra-strand rule of A = T and G = C. Journal of Molecular Evolution, 49(1), 53–58. https://doi.org/10.1007/PL00006534
• Sofia, M.J., Chang, W., Furman, P.A., Mosley, R.T., Ross, B.S. (2012). Nucleoside, nucleotide, and non-nucleoside inhibitors of Hepatitis C virus NS5B RNA-dependent RNA-polymerase. Journal of Medicinal Chemistry, 55, 2481–2531. https://doi.org/10.1021/jm201384j
• Sun, J., Zhao, W., Wang, R., Zhang, W., Li, G., Lu, M., Shao, Y., Yang, Y., Wang, N., Gao, Q., Su, S. (2020). Analysis of the codon usage pattern of HA and NA genes of H7N9 influenza a virus. International Journal of Molecular Sciences. 21(19), 7129. https://doi.org/10.3390/ijms21197129
• Suzuki, H., Brown, C.J., Forney, L.J., Top, E.M. (2008). Comparison of correspondence analysis methods for synonymous codon usage in bacteria. DNA Research, 15(6), 357–365. https://doi.org/10.1093/dnares/dsn028
• Tian, H. feng, Hu, Q. mu, Xiao, H. bing, Zeng, L. bing, Meng, Y., Li, Z. (2020). Genetic and codon usage bias analyses of major capsid protein gene in Ranavirus. Infection, Genetics and Evolution, 84(8), 1–13. https://doi.org/10.1016/j.meegid.2020.104379
• Tyagi, A., Kumar, B.T.N., Singh, N.K. (2017). Genome dynamics and evolution of codon usage patterns in shrimp viruses. Archives of Virology, 162(10), 3137–3142. https://doi.org/10.1007/s00705-017-3445-7
• Tyagi, A., Nagar, V. (2022). Genome dynamics, codon usage patterns and influencing factors in Aeromonas hydrophila phages. Virus Research, 320, 198900. https://doi.org/10.1016/j.virusres.2022.198900
• van Hemert, F., Berkhout, B. (2016). Nucleotide composition of the Zika virus RNA genome and its codon usage. Virology Journal. 13, 95. https://doi.org/10.1186/s12985-016-0551-1
• Wang, F., Zhang, N., Zhao, C., Song, Z., Xin, C. (2023). Codon usage bias analysis of mitochondrial protein-coding genes in 12 species of Candida. Journal of Genetics, 102(2), 36. https://doi.org/10.1007/s12041-023-01434-w
• Wang, H., Liu, S., Lv, Y., Wei, W. (2023). Codon usage bias of Venezuelan equine encephalitis virus and its host adaption. Virus Research, 328, 199081. https://doi.org/10.1016/j.virusres.2023.199081
• Wang, H., Meng, T., Wei, W. (2018). Analysis of synonymous codon usage bias in helicase gene from Autographa californica multiple nucleopolyhedrovirus. Genes and Genomics, 40(7), 767–780. https://doi.org/10.1007/s13258-018-0689-x
• Williams, T. (2008). Natural invertebrate hosts of iridoviruses (Iridoviridae). Neotrop Entomology, 37(6), 615–632. https://doi.org/10.1590/S1519-566X2008000600001
• Yang, S., Liu, Y., Wu, X., Cheng, X., Wu, X. (2022). Synonymous codon pattern of cowpea mild mottle virus sheds light on its host adaptation and genome evolution. Pathogens.11, 419. https://doi.org/10.3390/pathogens11040419
• Yannai, A., Katz, S., Hershberg, R. (2018). The codon usage of lowly expressed genes is subject to natural selection. Genome Biology and Evolution, 10(5), 1237–1246. https://doi.org/10.1093/gbe/evy084
• Yesilyurt, A., Muratoglu, H., Demirbag, Z., Nalcacioglu, R. (2019). Chilo iridescent virus encodes two functional metalloproteases. Archives of Virology, 164(3), 657–665. https://doi.org/10.1007/s00705-018-4108-z
• Zhang, J., Wang, M., Liu, W.Q., Zhou, J.H., Chen, H.T., Ma, L.N., Ding, Y.Z., Gu, Y.X., Liu, Y.S. (2011). Analysis of codon usage and nucleotide composition bias in polioviruses. Virology Journal, 8, 146. https://doi.org/10.1186/1743-422X-8-146
• Zhang, Y., Shen, Z., Meng, X., Zhang, L., Liu, Z., Liu, M., Zhang, F., Zhao, J. (2022). Codon usage patterns across seven Rosales species. BMC Plant Biology, 22(1), 1–10. https://doi.org/10.1186/s12870-022-03450-x
• Zhong, J., Li, Y., Zhao, S., Liu, S., Zhang, Z. (2007). Mutation pressure shapes codon usage in the GC-rich genome of foot-and-mouth disease virus. Virus Genes, 35(3), 767–776. https://doi.org/10.1007/s11262-007-0159-z
• Zhou, Y., Hou, Y., Shen, J., Huang, Y., Martin, W., Cheng, F. (2020). Network-based drug repurposing for novel coronavirus 2019-nCoV/SARS-CoV-2. Cell Discovery. 6,14. https://doi.org/10.1038/s41421-020-0153-3