Dynamic Molecular Epidemiology Reveals Lineage-Associated Single-Nucleotide Variants That Alter RNA Structure in Chikungunya Virus
Abstract
:1. Introduction
1.1. Geographical Spread of Chikungunya Virus
1.2. RNA Structure Conservation in Chikungunya Virus Genomes
1.3. Molecular Epidemiology Reveals RNA Structure-Affecting SNVs
2. Materials and Methods
2.1. Taxon Selection
2.2. Genetic Distance
2.3. CHIKV Nextstrain
2.4. RNA sTructure Modulation via Lineage-Associated SNVs
2.5. Data Availability
3. Results
3.1. Genetic Distance between Chikungunya Virus Lineages
3.2. A Nextstrain Build for Chikungunya Virus
3.3. Lineage-Specific RNA Structures
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Lineage | Divergence |
---|---|
AUL-Am | 0.0012 |
AUL | 0.0128 |
SAL | 0.003 |
MAL | 0.0107 |
IOL | 0.0062 |
EAL | 0.0011 |
AAL | 0.0066 |
WA | 0.0102 |
References
- Chandak, N.; Kashyap, R.; Kabra, D.; Karandikar, P.; Saha, S.; Morey, S.; Purohit, H.; Taori, G.; Daginawala, H. Neurological complications of Chikungunya virus infection. (Original Article) (Clinical report). Neurol. India 2009, 57, 177. [Google Scholar] [PubMed] [Green Version]
- Forrester, N.; Palacios, G.; Tesh, R.; Savji, N.; Guzman, H.; Sherman, M.; Weaver, S.; Lipkin, W. Genome-scale phylogeny of the alphavirus genus suggests a marine origin. J. Virol. 2011, 86, 2729–2738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weaver, S.C.; Forrester, N.L. Chikungunya: Evolutionary history and recent epidemic spread. Antivir. Res. 2015, 120, 32–39. [Google Scholar] [CrossRef]
- Her, Z.; Kam, Y.W.; Lin, R.T.; Ng, L.F. Chikungunya: A bending reality. Microbes Infect. 2009, 11, 1165–1176. [Google Scholar] [CrossRef]
- Robinson, M.C. An Epidemic Of Virus Disease In Southern Province, Tanganyika Territory. Trans. R. Soc. Trop. Med. Hyg. 1955, 49, 28–32. [Google Scholar] [CrossRef]
- Ross, R. The Newala epidemic: III. The virus: Isolation, pathogenic properties and relationship to the epidemic. Epidemiol. Infect. 1956, 54, 177–191. [Google Scholar] [CrossRef] [Green Version]
- Pialoux, G.; Gaüzère, B.A.; Jauréguiberry, S.; Strobel, M. Chikungunya, an epidemic arbovirosis. Lancet Infect. Dis. 2007, 7, 319–327. [Google Scholar] [CrossRef]
- Renault, P.; Solet, J.L.; Sissoko, D.; Balleydier, E.; Larrieu, S.; Filleul, L.; Lassalle, C.; Thiria, J.; Rachou, E.; De Valk, H.; et al. A major epidemic of chikungunya virus infection on Réunion Island, France, 2005–2006. Am. J. Trop. Med. Hyg. 2007, 77, 727–731. [Google Scholar] [CrossRef]
- Tsetsarkin, K.A.; Chen, R.; Weaver, S.C. Interspecies transmission and chikungunya virus emergence. Curr. Opin. Virol. 2016, 16, 143–150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schuffenecker, I.; Iteman, I.; Michault, A.; Murri, S.; Frangeul, L.; Vaney, M.C.; Lavenir, R.; Pardigon, N.; Reynes, J.M.; Pettinelli, F.; et al. Genome Microevolution of Chikungunya Viruses Causing the Indian Ocean Outbreak (Chikungunya Virus Genome Microevolution). PLoS Med. 2006, 3, e263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Centers for Disease Control and Prevention. Countries and Territories Where Chikungunya Cases Have Been Reported (as of 17 September 2019). 2019. Available online: https://www.cdc.gov/chikungunya/geo (accessed on 8 June 2020).
- Delatte, H.; Desvars, A.; Bouetard, A.; Bord, S.; Gimonneau, G.; Vourc, G.; Fontenille, D. Blood-feeding behavior of Aedes albopictus, a Vector of Chikungunya on la Reunion. (Report). Vector-Borne Zoonotic Dis. 2010, 10, 249. [Google Scholar] [CrossRef] [Green Version]
- Rochlin, I.; Ninivaggi, D.V.; Hutchinson, M.L.; Farajollahi, A. Climate change and range expansion of the Asian tiger mosquito (Aedes albopictus) in Northeastern USA: Implications for public health practitioners. PLoS ONE 2013, 8, e60874. [Google Scholar] [CrossRef]
- Powers, A.M.; Brault, A.C.; Tesh, R.B.; Weaver, S.C. Re-emergence of Chikungunya and O’nyong-nyong viruses: Evidence for distinct geographical lineages and distant evolutionary relationships. J. Gen. Virol. 2000, 81, 471–479. [Google Scholar] [CrossRef]
- Volk, S.M.; Chen, R.; Tsetsarkin, K.A.; Adams, A.P.; Garcia, T.I.; Sall, A.A.; Nasar, F.; Schuh, A.J.; Holmes, E.C.; Higgs, S.; et al. Genome-Scale Phylogenetic Analyses of Chikungunya Virus Reveal Independent Emergences of Recent Epidemics and Various Evolutionary Rates. J. Virol. 2010, 84, 6497–6504. [Google Scholar] [CrossRef] [Green Version]
- De Bernardi Schneider, A.; Ochsenreiter, R.; Hostager, R.; Hofacker, I.L.; Janies, D.; Wolfinger, M.T. Updated Phylogeny of Chikungunya Virus Suggests Lineage-Specific RNA Architecture. Viruses 2019, 11, 798. [Google Scholar] [CrossRef] [Green Version]
- Nunes, M.R.T.; Faria, N.R.; de Vasconcelos, J.M.; Golding, N.; Kraemer, M.U.; de Oliveira, L.F.; da Silva Azevedo, R.d.S.; da Silva, D.E.A.; da Silva, E.V.P.; da Silva, S.P.; et al. Emergence and potential for spread of Chikungunya virus in Brazil. BMC Med. 2015, 13, 102. [Google Scholar] [CrossRef] [Green Version]
- Teixeira, M.G.; Andrade, A.M.; Maria da Conceição, N.C.; Castro, J.S.; Oliveira, F.L.; Goes, C.S.; Maia, M.; Santana, E.B.; Nunes, B.T.; Vasconcelos, P.F. East/Central/South African genotype Chikungunya virus, Brazil, 2014. Emerg. Infect. Dis. 2015, 21, 906. [Google Scholar] [CrossRef] [Green Version]
- White, S.K.; Mavian, C.; Salemi, M.; Morris, J.G., Jr.; Elbadry, M.A.; Okech, B.A.; Lednicky, J.A.; Dunford, J.C. A new “American” subgroup of African-lineage Chikungunya virus detected in and isolated from mosquitoes collected in Haiti, 2016. PLoS ONE 2018, 13, e0196857. [Google Scholar] [CrossRef] [Green Version]
- Rezza, G.; Nicoletti, L.; Angelini, R.; Romi, R.; Finarelli, A.; Panning, M.; Cordioli, P.; Fortuna, C.; Boros, S.; Magurano, F.; et al. Infection with Chikungunya virus in Italy: An outbreak in a temperate region. Lancet 2007, 370, 1840–1846. [Google Scholar] [CrossRef]
- Lanciotti, R.S.; Kosoy, O.L.; Laven, J.J.; Panella, A.J.; Velez, J.O.; Lambert, A.J.; Campbell, G.L. Chikungunya virus in US travelers returning from India, 2006. Emerg. Infect. Dis. 2007, 13, 764. [Google Scholar] [CrossRef]
- De Lamballerie, X.; Leroy, E.; Charrel, R.; Ttsetsarkin, K.; Higgs, S.; Gould, E. Chikungunya virus adapts to tiger mosquito via evolutionary convergence: A sign of things to come? Virol. J. 2008, 5, 33. [Google Scholar] [CrossRef] [Green Version]
- Zeller, H.; Van Bortel, W.; Sudre, B. Chikungunya: Its history in Africa and Asia and its spread to new regions in 2013–2014. J. Infect. Dis. 2016, 214, S436–S440. [Google Scholar] [CrossRef]
- Yactayo, S.; Staples, J.E.; Millot, V.; Cibrelus, L.; Ramon-Pardo, P. Epidemiology of Chikungunya in the Americas. J. Infect. Dis. 2016, 214, S441–S445. [Google Scholar] [CrossRef] [Green Version]
- Halstead, S.B. Reappearance of chikungunya, formerly called dengue, in the Americas. Emerg. Infect. Dis. 2015, 21, 557. [Google Scholar] [CrossRef] [Green Version]
- Strauss, J.H.; Strauss, E.G. The Alphaviruses: Gene Expression, Replication, and Evolution. Microbiol. Mol. Biol. R. 1994, 58, 491–562. [Google Scholar] [CrossRef]
- Li, X.F.; Jiang, T.; Deng, Y.Q.; Zhao, H.; Yu, X.D.; Ye, Q.; Wang, H.J.; Zhu, S.Y.; Zhang, F.C.; Qin, E.D.; et al. Complete genome sequence of a Chikungunya virus isolated in Guangdong, China. J. Virol. 2012, 86, 8904–8905. [Google Scholar] [CrossRef] [Green Version]
- Hyde, J.L.; Chen, R.; Trobaugh, D.W.; Diamond, M.S.; Weaver, S.C.; Klimstra, W.B.; Wilusz, J. The 5’ and 3’ ends of alphavirus RNAs–non-coding is not non-functional. Virus Res. 2015, 206, 99–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, R.; Wang, E.; Tsetsarkin, K.A.; Weaver, S.C. Chikungunya virus 3’ untranslated region: Adaptation to mosquitoes and a population bottleneck as major evolutionary forces. PLoS Pathog. 2013, 9, e1003591. [Google Scholar] [CrossRef] [Green Version]
- Filomatori, C.V.; Bardossy, E.S.; Merwaiss, F.; Suzuki, Y.; Henrion, A.; Saleh, M.C.; Alvarez, D.E. RNA recombination at Chikungunya virus 3’UTR as an evolutionary mechanism that provides adaptability. PLoS Pathog. 2019, 15, e1007706. [Google Scholar] [CrossRef]
- Kiening, M.; Ochsenreiter, R.; Hellinger, H.J.; Rattei, T.; Hofacker, I.; Frishman, D. Conserved secondary structures in viral mRNAs. Viruses 2019, 11, 401. [Google Scholar] [CrossRef] [Green Version]
- Ochsenreiter, R.; Hofacker, I.L.; Wolfinger, M.T. Functional RNA Structures in the 3’UTR of Tick-Borne, Insect-Specific and No-Known-Vector Flaviviruses. Viruses 2019, 11, 298. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, D.; Leibowitz, J.L. The structure and functions of coronavirus genomic 3’ and 5’ ends. Virus Res. 2015, 206, 120–133. [Google Scholar] [CrossRef]
- Kutchko, K.M.; Madden, E.A.; Morrison, C.; Plante, K.S.; Sanders, W.; Vincent, H.A.; Cruz Cisneros, M.C.; Long, K.M.; Moorman, N.J.; Heise, M.T.; et al. Structural divergence creates new functional features in alphavirus genomes. Nucleic Acids Res. 2018, 46, 3657–3670. [Google Scholar] [CrossRef] [Green Version]
- Madden, E.A.; Plante, K.S.; Morrison, C.R.; Kutchko, K.M.; Sanders, W.; Long, K.M.; Taft-Benz, S.; Cisneros, M.C.C.; White, A.M.; Sarkar, S.; et al. Using SHAPE-MaP to model RNA secondary structure and identify 3’UTR variation in chikungunya virus. J. Virol. 2020, 94, e00701-20. [Google Scholar] [CrossRef] [PubMed]
- Pfeffer, M.; Kinney, R.M.; Kaaden, O.R. The Alphavirus 3’-Nontranslated Region: Size Heterogeneity and Arrangement of Repeated Sequence Elements. Virology 1998, 240, 100–108. [Google Scholar] [CrossRef] [Green Version]
- Halvorsen, M.; Martin, J.S.; Broadaway, S.; Laederach, A. Disease-associated mutations that alter the RNA structural ensemble. PLoS Genet. 2010, 6, e1001074. [Google Scholar] [CrossRef] [Green Version]
- Martin, J.S.; Halvorsen, M.; Davis-Neulander, L.; Ritz, J.; Gopinath, C.; Beauregard, A.; Laederach, A. Structural effects of linkage disequilibrium on the transcriptome. RNA 2012, 18, 77–87. [Google Scholar] [CrossRef] [Green Version]
- Wan, Y.; Qu, K.; Zhang, Q.C.; Flynn, R.A.; Manor, O.; Ouyang, Z.; Zhang, J.; Spitale, R.C.; Snyder, M.P.; Segal, E.; et al. Landscape and variation of RNA secondary structure across the human transcriptome. Nature 2014, 505, 706–709. [Google Scholar] [CrossRef] [Green Version]
- Corley, M.; Solem, A.; Qu, K.; Chang, H.Y.; Laederach, A. Detecting riboSNitches with RNA folding algorithms: A genome-wide benchmark. Nucleic Acid Res. 2015, 43, 1859–1868. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, F.; Wei, R.; Zhou, Z.; Huang, L.; Wang, Y.; Tang, J.; Zou, Y.; Shi, L.; Gu, X.; Davis, M.J.; et al. Integrative Analysis of Somatic Mutations in Non-coding Regions Altering RNA Secondary Structures in Cancer Genomes. Sci. Rep. 2019, 9, 1–12. [Google Scholar] [CrossRef]
- Lin, J.; Chen, Y.; Zhang, Y.; Ouyang, Z. Identification and analysis of RNA structural disruptions induced by single nucleotide variants using Riprap and RiboSNitchDB. NAR Genom. Bioinform. 2020, 2, lqaa057. [Google Scholar] [CrossRef]
- De Bernardi Schneider, A.; Ford, C.T.; Hostager, R.; Williams, J.; Cioce, M.; Çatalyürek, Ü.V.; Wertheim, J.O.; Janies, D. StrainHub: A phylogenetic tool to construct pathogen transmission networks. Bioinformatics 2020, 36, 945–947. [Google Scholar] [CrossRef]
- Campbell, F.; Didelot, X.; Fitzjohn, R.; Ferguson, N.; Cori, A.; Jombart, T. outbreaker2: A modular platform for outbreak reconstruction. BMB Bioinform. 2018, 19, 1–8. [Google Scholar] [CrossRef] [Green Version]
- De Maio, N.; Worby, C.J.; Wilson, D.J.; Stoesser, N. Bayesian reconstruction of transmission within outbreaks using genomic variants. PLoS Comput. Biol. 2018, 14, e1006117. [Google Scholar] [CrossRef] [Green Version]
- Hadfield, J.; Megill, C.; Bell, S.M.; Huddleston, J.; Potter, B.; Callender, C.; Sagulenko, P.; Bedford, T.; Neher, R.A. Nextstrain: Real-time tracking of pathogen evolution. Bioinformatics 2018, 34, 4121–4123. [Google Scholar] [CrossRef]
- Kinganda-Lusamaki, E.; Black, A.; Mukadi, D.; Hadfield, J.; Mbala-Kingebeni, P.; Pratt, C.; Aziza, A.; Diagne, M.; White, B.; Bisento, N.; et al. Operationalizing genomic epidemiology during the Nord-Kivu Ebola outbreak, Democratic Republic of the Congo. medRxiv 2020. [Google Scholar] [CrossRef]
- Popa, A.; Genger, J.W.; Nicholson, M.D.; Penz, T.; Schmid, D.; Aberle, S.W.; Agerer, B.; Lercher, A.; Endler, L.; Colaco, H.; et al. Genomic epidemiology of superspreading events in Austria reveals mutational dynamics and transmission properties of SARS-CoV-2. Sci. Transl. Med. 2020, 12. [Google Scholar] [CrossRef] [PubMed]
- Clark, K.; Karsch-Mizrachi, I.; Lipman, D.J.; Ostell, J.; Sayers, E.W. GenBank. Nucleic Acids Res. 2016, 44, D67–D72. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- Tamura, K.; Nei, M.; Kumar, S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 2004, 101, 11030–11035. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Köster, J.; Rahmann, S. Snakemake—A scalable bioinformatics workflow engine. Bioinformatics 2012, 28, 2520–2522. [Google Scholar] [CrossRef] [Green Version]
- Lorenz, R.; Stadler, P.F. RNA Secondary Structures with Limited Base Pair Span: Exact Backtracking and an Application. Genes 2021, 12, 14. [Google Scholar] [CrossRef] [PubMed]
- Lorenz, R.; Bernhart, S.H.; Zu Siederdissen, C.H.; Tafer, H.; Flamm, C.; Stadler, P.F.; Hofacker, I.L. ViennaRNA Package 2.0. Algorithm. Mol. Biol. 2011, 6, 26. [Google Scholar] [CrossRef]
- Miladi, M.; Raden, M.; Diederichs, S.; Backofen, R. MutaRNA: Analysis and visualization of mutation-induced changes in RNA structure. Nucleic Acids Res. 2020, 37, 1–5. [Google Scholar] [CrossRef]
- Sagulenko, P.; Puller, V.; Neher, R.A. TreeTime: Maximum-likelihood phylodynamic analysis. Virus Evol. 2018, 4, vex042. [Google Scholar] [CrossRef]
- Lopez-Delisle, L.; Rabbani, L.; Wolff, J.; Bhardwaj, V.; Backofen, R.; Grüning, B.; Ramírez, F.; Manke, T. pyGenomeTracks: Reproducible plots for multivariate genomic data sets. Bioinformatics 2020, btaa692. [Google Scholar] [CrossRef] [PubMed]
- Tsetsarkin, K.A.; Vanlandingham, D.L.; McGee, C.E.; Higgs, S. A single mutation in Chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 2007, 3, e201. [Google Scholar] [CrossRef]
- McNaughton, A.L.; Revill, P.A.; Littlejohn, M.; Matthews, P.C.; Ansari, M.A. Analysis of genomic-length HBV sequences to determine genotype and subgenotype reference sequences. J. Gen. Virol. 2020, 101, 1–13. [Google Scholar] [CrossRef]
- Bbosa, N.; Kaleebu, P.; Ssemwanga, D. HIV subtype diversity worldwide. Curr. Opin. HIV Aids 2019, 14, 153–160. [Google Scholar] [CrossRef]
- De Bernardi Schneider, A.; Osiowy, C.; Hostager, R.; Krarup, H.; Borresen, M.; Tanaka, Y.; Morriseau, T.; Wertheim, J.O. Analysis of Hepatitis B virus genotype D in Greenland suggests the presence of a novel quasi-subgenotype. Front. Microbiol. 2021. [Google Scholar] [CrossRef]
- Robertson, D.L.; Anderson, J.; Bradac, J.; Carr, J.; Foley, B.; Funkhouser, R.; Gao, F.; Hahn, B.; Kalish, M.; Kuiken, C.; et al. HIV-1 nomenclature proposal. Science 2000, 288, 55–56. [Google Scholar] [CrossRef]
- Souza, T.M.A.; Azeredo, E.L.; Badolato-Corrêa, J.; Damasco, P.V.; Santos, C.; Petitinga-Paiva, F.; Nunes, P.C.G.; Barbosa, L.S.; Cipitelli, M.C.; Chouin-Carneiro, T.; et al. First report of the East-Central South African genotype of Chikungunya virus in Rio de Janeiro, Brazil. PLoS Curr. 2017, 9. [Google Scholar] [CrossRef]
- Schuster, P. Quasispecies on Fitness Landscapes. In Quasispecies: From Theory to Experimental Systems; Domingo, E., Schuster, P., Eds.; Springer International Publishing: Cham, Switzerland, 2016; pp. 61–120. [Google Scholar] [CrossRef]
- Geoghegan, J.L.; Holmes, E.C. Virus Evolution. In Fields Virology; Howley, P.M., Knipe, D.M., Eds.; Wolters Kluwer Health: Philadelphia, PA, USA, 2021. [Google Scholar]
- Faure, G.; Ogurtsov, A.Y.; Shabalina, S.A.; Koonin, E.V. Adaptation of mRNA structure to control protein folding. RNA Biol. 2017, 14, 1649–1654. [Google Scholar] [CrossRef]
Lineage | AUL-Am | AUL | SAL | MAL | IOL | EAL | AAL | sECSA |
---|---|---|---|---|---|---|---|---|
AUL | 0.01108 | |||||||
SAL | 0.06902 | 0.06622 | ||||||
MAL | 0.06840 | 0.06548 | 0.02432 | |||||
IOL | 0.06988 | 0.06734 | 0.02954 | 0.02631 | ||||
EAL | 0.06763 | 0.06533 | 0.02574 | 0.02259 | 0.00584 | |||
AAL | 0.06390 | 0.06067 | 0.03145 | 0.02887 | 0.03141 | 0.02807 | ||
sECSA | 0.06302 | 0.06014 | 0.02957 | 0.02758 | 0.03038 | 0.02690 | 0.01918 | |
WA | 0.19383 | 0.19228 | 0.17696 | 0.17829 | 0.17917 | 0.17750 | 0.17443 | 0.17505 |
Lineage | TMRCA | Date Confidence Interval | Year of First Isolation |
---|---|---|---|
AAL | 17-04-1948 | (18-10-1946,14-12-1949) | 1953 |
AUL | 05-02-1951 | (13-09-1949, 04-01-1953) | 1958 |
AUL-Am | 12-03-2008 | (24-12-2007, 10-11-2008) | 2013 |
EAL | 24-05-2002 | (15-02-2001, 20-04-2003) | 2005 |
IOL | 03-08-2003 | (20-10-2002, 14-01-2004) | 2006 |
MAL | 31-01-1953 | (20-05-1951, 14-01-1955) | 1962 |
SAL | 22-03-2011 | (24-06-2009, 15-09-2012) | 2014 |
WA | 16-01-1954 | (13-05-1952, 26-09-1955) | 1964 |
Variant | Type | Protein | AA Mutation | RNA # | Locus | z-Score | BP Distance | Lineage Association | ||
---|---|---|---|---|---|---|---|---|---|---|
G432A | N | nsP1 | E > A | 1 | 378–472 | −30.00 | −2.474 | −27.00 | 29 | G: AUL, AUL-Am |
U810C | S | nsP1 | – | 2 | 783–847 | −21.60 | −2.103 | −18.70 | 42 | U: WA, AUL, AUL-Am, * |
A1653G | S | nsP1 | – | 3 | 1605–1685 | −23.30 | −2.640 | −28.10 | 15 | A: AUL , AUL-Am |
U2122C | S | nsP2 | – | 4 | 2105–2202 | −31.90 | −2.171 | −28.30 | 29 | U: AUL, AUL-Am |
G2232A | S | nsP2 | – | 5 | 2210–2300 | −31.50 | −2.771 | −27.40 | 36 | G: AUL, AUL-Am |
C3108U | S | nsP2 | – | 6 | 3093–3192 | −28.20 | −2.141 | −25.60 | 42 | C: WA, AUL, AUL-Am |
C3682U | S | nsP2 | – | 7 | 3630–3731 | −42.20 | −4.325 | −40.10 | 22 | C: AUL, AUL-Am, * |
U5508A | N | nsP3 | D > E | 8 | 5467–5527 | −18.10 | −2.370 | −16.20 | 15 | U: , AUL-Am |
G8336C | S | C | – | 9 | 8312–8395 | −37.10 | −3.023 | −34.40 | 27 | G: , AUL-Am |
C8358U | S | C | – | 9 | 8312–8395 | −37.10 | −3.023 | −36.40 | 27 | C: AUL, AUL-AM, SAL, MAL , * |
G8969A | N | E2 | R > K | 10 | 8918–9019 | −38.60 | −2.447 | −36.10 | 40 | A: , AUL-Am |
C9197U | S | E2 | – | 11 | 9130–9214 | −22.40 | −2.443 | −20.40 | 34 | C: WA, AUL, AUL-AM |
A9414C | S | E2 | – | 12 | 9392–9456 | −17.60 | −2.568 | −15.80 | 18 | A: , AUL-Am |
A10460C | N | E1 | I > V | 13 | 10369–10468 | −31.60 | −2.623 | −31.70 | 18 | A: AUL, AUL-AM |
A11246C | S | E1 | – | 14 | 11,228–11,307 | −29.30 | −3.049 | −26.90 | 25 | A: AUL, AUL-Am, AAL, SAL, MAL; C: EAL, IOL |
A11246U | S | E1 | – | 14 | 11,228–11,307 | −29.30 | −3.049 | −27.20 | 36 | A: AUL, AUL-Am, AAL, SAL, MAL; U: WA |
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Spicher, T.; Delitz, M.; Schneider, A.d.B.; Wolfinger, M.T. Dynamic Molecular Epidemiology Reveals Lineage-Associated Single-Nucleotide Variants That Alter RNA Structure in Chikungunya Virus. Genes 2021, 12, 239. https://doi.org/10.3390/genes12020239
Spicher T, Delitz M, Schneider AdB, Wolfinger MT. Dynamic Molecular Epidemiology Reveals Lineage-Associated Single-Nucleotide Variants That Alter RNA Structure in Chikungunya Virus. Genes. 2021; 12(2):239. https://doi.org/10.3390/genes12020239
Chicago/Turabian StyleSpicher, Thomas, Markus Delitz, Adriano de Bernardi Schneider, and Michael T. Wolfinger. 2021. "Dynamic Molecular Epidemiology Reveals Lineage-Associated Single-Nucleotide Variants That Alter RNA Structure in Chikungunya Virus" Genes 12, no. 2: 239. https://doi.org/10.3390/genes12020239
APA StyleSpicher, T., Delitz, M., Schneider, A. d. B., & Wolfinger, M. T. (2021). Dynamic Molecular Epidemiology Reveals Lineage-Associated Single-Nucleotide Variants That Alter RNA Structure in Chikungunya Virus. Genes, 12(2), 239. https://doi.org/10.3390/genes12020239