Analysis of the genetic features of the structural organization of integrative conjugative elements of Vibrio cholerae strains of various origins

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Background: Integrative conjugative elements (ICEs) play a significant role in the dissemination of antibiotic resistance genes among Vibrio cholerae strains. However, there are currently no standardized methods for ICE typing that allow for the analysis of large genomic datasets.

Aim: To conduct a comparative analysis of ICE sequences in Vibrio cholerae strains of various origins and to develop an algorithm for their typing.

Materials and methods: The study utilized whole-genome sequencing data from 120 toxigenic (ctxAB+tcpA+) V. cholerae O1 El Tor strains obtained using the MiSeq platform (Illumina, USA) and MinION platform (Oxford Nanopore, UK), as well as data from NCBI databases (1,886 genomes) and the European Nucleotide Archive (441 strains). The software for ICE detection and typing was developed in Java (version 11.0.13) and is available at: http://antiplague.ru/ice-genotyper/.

Results: A comparative analysis of ICE elements in toxigenic V. cholerae strains was performed. An ICE typing algorithm based on gene composition was proposed. Analysis of the V. cholerae genome collection revealed three previously undescribed ICE elements, designated ICEVchRus1, ICEVchHai3, and ICEVchLaos.

Conclusions: The study identified three previously undescribed ICE elements and mapped their distribution across Russia and other regions of the world. It was established that during the cholera outbreak in Dagestan in 1994, strains containing ICEVchBan11 and ICEVchBan9 were circulating simultaneously.

Full Text

Restricted Access

About the authors

Alexey S. Vodopyanov

Rostov-on-Don Plague Control Researsh Institute

Author for correspondence.
Email: vodopyanov_as@antiplague.ru
ORCID iD: 0000-0002-9056-3231
SPIN-code: 7319-3037

MD, Cand. Sci. (Medicine)

Russian Federation, Rostov-on-Don

Ruslan V. Pisanov

Rostov-on-Don Plague Control Researsh Institute

Email: plague@aaanet.ru
ORCID iD: 0000-0002-7178-8021
SPIN-code: 4270-3091

Cand. Sci. (Biology)

Russian Federation, Rostov-on-Don

Sergey O. Vodopyanov

Rostov-on-Don Plague Control Researsh Institute

Email: serge100v@gmail.com
ORCID iD: 0000-0003-4336-0439
SPIN-code: 4672-9310

MD, Dr. Sci. (Medicine)

Russian Federation, Rostov-on-Don

Aleksey K. Noskov

Rostov-on-Don Plague Control Researsh Institute

Email: noskov-epid@mail.ru
ORCID iD: 0000-0003-0550-2221
SPIN-code: 5378-3729

MD, Cand. Sci. (Medicine)

Russian Federation, Rostov-on-Don

References

  1. Rybal’chenko DA, Shchelkanova EYu, Lozovsky YuV, et al. Prevalence of Different Types of Integrative Conjugative Element SXT/R391 Encoding Multiple Antibiotic Resistance Among Clinical Strains of Cholera Agent. Problems of Particularly Dangerous Infections. 2022;(1):137–147. doi: 10.21055/0370-1069-2022-1-137-147
  2. Smirnova NI, Rybal’chenko DA, Shchelkanova EYu, et al. Variability of multiple resistance to antibiotics in cholera agent associated with different types of SXT element and spontaneous chromosome mutations. Molecular Genetics, Microbiology and Virology. 2022;40(2):28–36. doi: 10.17116/molgen20224002128
  3. Das B, Verma J, Kumar P, et al. Antibiotic resistance in Vibrio cholerae: Understanding the ecology of resistance genes and mechanisms. Vaccine. 2020;38 Suppl. 1:A83–A92. doi: 10.1016/j.vaccine.2019.06.031
  4. Selyanskaya NA, Vodop’yanov SO, Rykova VA, Sokolova EP. Transmissive Antibiotic Resistance, Associated with the SXT Element, in Cholera Vibrios Isolated in the Territory of Russia. Journal of Microbiology, Epidemiology and Immunobiology. 2020;97(3):258–264. doi: 10.36233/0372-9311-2020-97-3-8
  5. Pant A, Bag S, Saha B, et al. Molecular insights into the genome dynamics and interactions between core and acquired genomes of Vibrio cholerae. Proc Natl Acad Sci U S A. 2020;117(38):23762–23773. doi: 10.1073/pnas.2006283117
  6. Wang P, Zhao Y, Wang W, et al. Mobile genetic elements used by competing coral microbial populations increase genomic plasticity. ISME J. 2022;16(9):2220–2229. doi: 10.1038/s41396-022-01272-1
  7. Wozniak RA, Fouts DE, Spagnoletti M, et al. Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet. 2009;5(12):e1000786. doi: 10.1371/journal.pgen.1000786
  8. Marin MA, Fonseca EL, Andrade BN, et al. Worldwide occurrence of integrative conjugative element encoding multidrug resistance determinants in epidemic Vibrio cholerae O1. PLoS One. 2014;9(9):e108728. doi: 10.1371/journal.pone.0108728
  9. Ceccarelli D, Spagnoletti M, Hasan NA, et al. A new integrative conjugative element detected in Haitian isolates of Vibrio cholerae non-O1/non-O139. Res Microbiol. 2013;164(9):891–893. doi: 10.1016/j.resmic.2013.08.004
  10. Burrus V, Quezada-Calvillo R, Marrero J, Waldor MK. SXT-related integrating conjugative element in New World Vibrio cholerae. Appl Environ Microbiol. 2006;72(4):3054–3057. doi: 10.1128/AEM.72.4.3054-3057.2006
  11. Taviani E, Grim CJ, Chun J, et al. Genomic analysis of a novel integrative conjugative element in Vibrio cholerae. FEBS Lett. 2009;583(22):3630–3636. doi: 10.1016/j.febslet.2009.10.041
  12. Taviani E, Spagnoletti M, Ceccarelli D, et al. Genomic analysis of ICEVchBan8: An atypical genetic element in Vibrio cholerae. FEBS Lett. 2012;586(11):1617–1621. doi: 10.1016/j.febslet.2012.03.064
  13. Wang R, Yu D, Yue J, Kan B. Variations in SXT elements in epidemic Vibrio cholerae O1 El Tor strains in China. Sci Rep. 2016;6:22733. doi: 10.1038/srep22733
  14. Bankevich A, Nurk S, Antipov D, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–477. doi: 10.1089/cmb.2012.0021
  15. Vodopyanov AS, Vodopyanov SO, Mishan’kin BN, Olejnikov IP. Computer VNTR-genotyping algorithm based on the partial sequence data of Vibrio cholerae strains from Haitian outbreak (2010). Public health and life environment. 2013;(3):28–30. EDN: PXLUAZ
  16. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007;23(6):673–679. doi: 10.1093/bioinformatics/btm009
  17. Camacho C, Coulouris G, Avagyan V, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421
  18. Shimoyama Y. pyGenomeViz: A genome visualization python package for comparative genomics [Computer software]. 2022. Available from: https://github.com/moshi4/pyGenomeViz Accessed: 15 Jun 2024.
  19. Liu M, Li X, Xie Y, et al. ICEberg 2.0: an updated database of bacterial integrative and conjugative elements. Nucleic Acids Res. 2019;47(D1):D660–D665. doi: 10.1093/nar/gky1123
  20. Spagnoletti M, Ceccarelli D, Colombo MM. Rapid detection by multiplex PCR of Genomic Islands, prophages and Integrative Conjugative Elements in V. cholerae 7th pandemic variants. J Microbiol Methods. 2012;88(1):98–102. doi: 10.1016/j.mimet.2011.10.017
  21. Hochhut B, Beaber JW, Woodgate R, Waldor MK. Formation of chromosomal tandem arrays of the SXT element and R391, two conjugative chromosomally integrating elements that share an attachment site. J Bacteriol. 2001;183(4):1124–1132. doi: 10.1128/JB.183.4.1124-1132.2001
  22. Gladkikh AS, Feranchuk SI, Ponomareva AS, et al. Antibiotic resistance in Vibrio cholerae El Tor strains isolated during cholera complications in Siberia and the Far East of Russia. Infect Genet Evol. 2020;78:104096. doi: 10.1016/j.meegid.2019.104096
  23. Chaguza C, Chibwe I, Chaima D, et al. Genomic insights into the 2022–2023 Vibrio cholerae outbreak in Malawi. Nat Commun. 2024;15(1):6291. doi: 10.1038/s41467-024-50484-w
  24. Spagnoletti M, Ceccarelli D, Rieux A, et al. Acquisition and evolution of SXT-R391 integrative conjugative elements in the seventh-pandemic Vibrio cholerae lineage. mBio. 2014;5(4):e01356-14. doi: 10.1128/mBio.01356-14
  25. Kutar BM, Rajpara N, Upadhyay H, et al. Clinical isolates of Vibrio cholerae O1 El Tor Ogawa of 2009 from Kolkata, India: preponderance of SXT element and presence of Haitian ctxB variant. PLoS One. 2013;8(2):e56477. doi: 10.1371/journal.pone.0056477
  26. Weill FX, Domman D, Njamkepo E, et al. Genomic history of the seventh pandemic of cholera in Africa. Science. 2017;358(6364):785–789. doi: 10.1126/science.aad5901
  27. Sarkar A, Morita D, Ghosh A, et al. Altered Integrative and Conjugative Elements (ICEs) in Recent Vibrio cholera O1 Isolated From Cholera Cases, Kolkata, India. Front Microbiol. 2019;10:2072. doi: 10.3389/fmicb.2019.02072
  28. Monir MM, Hossain T, Morita M, et al. Genomic Characteristics of Recently Recognized Vibrio cholerae El Tor Lineages Associated with Cholera in Bangladesh, 1991 to 2017. Microbiol Spectr. 2022;10(2):e0039122. doi: 10.1128/spectrum.00391-22

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Comparative analysis of ICE elements ICEVchRus1 and ICEVchInd5.

Download (1MB)
Indexing metadata
3. Fig. 2. Comparative analysis of ICE elements ICEVchLaos and ICEVchCHN4210.

Download (1MB)
Indexing metadata
4. Fig. 3. Comparative analysis of ICE elements ICEVchInd5 and ICEVchHai3.

Download (1MB)
Indexing metadata
5. Fig. 4. Places and years of isolation of cholera vibrio strains containing ICEVchRus1.

Download (868KB)
Indexing metadata

Copyright (c) 2024 Eco-vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ЭЛ № ФС 77 - 80652 от 15.03.2021 . Учредитель ООО "Эко-Вектор Ай-Пи" (ОГРН 1157847215338).