https://doi.org/10.4081/jbr.2023.11202
Genetic characterization of non-O1/non-O139 Vibrio cholerae mobilome: a strategy for understanding and discriminating emerging environmental bacterial strains
Submitted: January 21, 2023
Accepted: June 14, 2023
Published: September 12, 2023
Accepted: June 14, 2023
Abstract Views: 944
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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Acute diarrhea and cholera (AWD/C) result in more than 21000 to 143000 global mortality annually and are associated with Vibrio cholerae. The pathogen has shown increasing evolutionary/emerging dynamics linked with mobilome or ubiquitous nature of mobile integrative genetic and conjugative elements (MIGCE), however, such dynamics are rarely reported amongst somatic-antigen non-agglutinating Type-1/-139 V. cholerae (SA-NAG-T-1/139Vc). The study reports the genetic detection of mobilome-associated indices in SA-NAG-T-1/139Vc as a potential strategy for differentiating/discriminating emerging environmental bacteria. Presumptive V. cholerae isolates were retrieved from five water sources, while strains were characterized/serogrouped and confirmed using simplex and comparative-genomic-multiplex Polymerase Chain Reaction (PCR). Genomic island (GI-12det, GI-14det, GI-15det); Phages (TLC-phagedet, Kappa-phagedet) and ICEs of the SXT/R391 family genes (SXT/R391-ICEs integrase, SXT-Hotspot-IV, ICEVchInd5Hotspot-IV, ICEVchMoz10Hotspot-IV) were detected. Other rare ICE members such as the ICEVcBan8att gene and Vibrio Seventh Pandemic island detection (VSP-II Integrase, Prototypical VSP-II) were also detected. Results revealed that the 8.22% (61/742) SA-NAG-T-1/139Vc serogroup observed harbors the Vibrio Seventh Pandemic island integrase (34/61; 55.7%) and other rare genetic traits including; attB/attP (29/61; 47.5%, 14/61; 23%), integrative genetic elements (4/61; 6.56%), phage types (TLC-phagedet: 2/61; 3.28% and Kappa-phagedet: 7/61; 11.48%) as well as the integrase genes (INT1, Sul1, Sul2) (29/61: 47.5%; 21/61: 34.4%; 25/61: 41%). Such genetic detection of mobilome determinants/MIGCE suggests potential discriminatory tendencies amongst SA-NAG-T-1/139Vcwhich may be applied in mobilome typing of evolving/emerging environmental bacteria. The need to encourage the application of such mobilome typing indices and continuous study of these strains is suggestive of interest in controlling future potential emerging environmental strains.
WHO-UNICEF, Strategic Framework for Cholera in Eastern and Southern Africa: 2017. Draft final for RMT consultation. 2018-2022. Available from: http://apps.who.int/data
Thomas L, Anandan S, Verghese VP, et al. Clinical characteristics, laboratory profile and outcome of children with Vibrio cholerae gastroenteritis (both O1 and Non-O1/Non-O139) and Vibrio cholerae (Non-O1/Non-O139) bacteraemia -A retrospective single centre study. J Clin Diagn Res 2020;14:SC01-6.
DOI: https://doi.org/10.7860/JCDR/2020/43621.13647
Igere BE, Okoh AI, Nwodo UU. Atypical and dual biotypes variant of virulent SA-NAG-Vibrio cholerae: an evidence of emerging/evolving patho-significant strain in municipal domestic water sources. Ann Microbiol 2022;72:1-13.
DOI: https://doi.org/10.1186/s13213-021-01661-5
World Health Organization Cholera. In: Fact Sheet №107. WHO, Geneva. 2016. (updated October 2016). Available from: http://www.who.int/mediacentre/factsheets/fs107/en/
Russini V, Giancola ML, Brunetti G, et al. A Cholera case imported from Bangladesh to Italy: Clinico-epidemiological management and molecular characterization in a non-endemic country. Trop Med Infect Dis 2023;8:266.
DOI: https://doi.org/10.3390/tropicalmed8050266
WHO-UNICEF. Strategic framework for cholera in Eastern and Southern Africa: 2018-2022 Draft final for RMT consultation. 2017.
Centers for Disease Control and Prevention (CDC). Cholera and other Vibrio illness surveillance overview. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2012.Accessed November 1, 2013. Authors: http://www.cdc.gov/ncezid/dfwed/PDFs/nat-covissurv-overview-508c.pdf.
Fernández-Abreu A, Bravo-Fariñas L, Rivero-Navea G, et al. Determinants of virulence and antimicrobial susceptibility in Non-O1, Non-O139 Vibrio cholerae isolates. MEDICC Rev 2017;19:21-5.
DOI: https://doi.org/10.37757/MR2017.V19.N4.6
Igere BE, Okoh AI, Nwodo UU. Non-serogroup O1/O139 agglutinable Vibrio cholerae: a phylogenetically and genealogically neglected yet emerging potential pathogen of clinical relevance. Arch Microbiol 2022;204:1-28.
DOI: https://doi.org/10.1007/s00203-022-02866-1
Banerjee R, Das B, Nair GB, Basak S. Dynamics in genome evolution of Vibrio cholerae. Infect Genet Evol 2014;23:32-41.
DOI: https://doi.org/10.1016/j.meegid.2014.01.006
Opintan JA, Newman MJ, Nsiah-Poodoh OA, Okeke IN. Vibrio cholerae O1 from Accra, Ghana carrying a class 2 integron and the SXT element. J Antimicrob Chemother 2008;62:929-33.
DOI: https://doi.org/10.1093/jac/dkn334
Canto de Sá LL, Lourenço da Fonseca E, Pellegrini M, et al. Occurrence and composition of class 1 and class 2 integrons in clinical and environmental O1 and non-O1/non-O139 Vibrio cholerae strains from the Brazilian Amazon. Mem Inst Oswaldo Cruz 2010;105:229-32.
DOI: https://doi.org/10.1590/S0074-02762010000200021
Igere BE, Onohuean H, Nwodo UU. Water bodies are potential hub for spatio-allotment of cell-free nucleic acid and pandemic: a pentadecadal (1969–2021) critical review on particulate cell-free DNA reservoirs in water nexus. Bull Natl Res Cent 2022;46:56.
DOI: https://doi.org/10.1186/s42269-022-00750-y
Gogarten MB, Gogarten JP, Olendzenski L, eds. Horizontal gene transfer: genomes in flux, vol. 532 C. New York: Humana Press, a part of Springer Science+Business Media, LLC 2009.
DOI: https://doi.org/10.1007/978-1-60327-853-9
Bellanger X, Payot S, Leblond-Bourget N, Guédon G. Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. FEMS Microbiol Rev 2014;38:720-60.
DOI: https://doi.org/10.1111/1574-6976.12058
Carraro N, Rivard N, Burrus V, Ceccarelli D. Mobilizable genomic islands, different strategies for the dissemination of multidrug resistance and other adaptive traits. Mobi Gene Elem 2017;7:1-6.
DOI: https://doi.org/10.1080/2159256X.2017.1304193
Daccord A, Ceccarelli D, Burrus V. Integrating conjugative elements of the SXT/R391 family trigger the excision and drive the mobilization of a new class of Vibrio genomic islands. Molecular Microbiol 2010;78:576-88.
DOI: https://doi.org/10.1111/j.1365-2958.2010.07364.x
Grim CJ, Hasan NA, Taviani E, et al. Genome Sequence of Hybrid Vibrio cholerae O1 MJ-1236, B-33, and CIRS101 and comparative genomics with V. cholerae. J Bacteriol 2010;192:3524-33.
DOI: https://doi.org/10.1128/JB.00040-10
Safa A, Nair GB, Kong RY. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol 2010;18:46-54.
DOI: https://doi.org/10.1016/j.tim.2009.10.003
Taviani E, Spagnoletti M, Ceccarelli D, et al. Genomic analysis of ICEVchBan8: An atypical genetic element in Vibrio cholerae. FEBS letters 2012;4;586:1617-21.
DOI: https://doi.org/10.1016/j.febslet.2012.03.064
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;19:e01356-14.
DOI: https://doi.org/10.1128/mBio.01356-14
Huq A, Haley BJ, Taviani E, et al. Detection, isolation, and identification of Vibrio cholerae from the environment. Curr Prot Microbiol 2012;26:6A-5.
DOI: https://doi.org/10.1002/9780471729259.mc06a05s26
Yong L, Guanpin Y, Hualei W, et al. Design ofVibrio 16S rRNA gene specific primers and their application in the analysis of seawaterVibrio community. J Ocean Univ China 2006;5:157-64.
DOI: https://doi.org/10.1007/BF02919216
Kalendar R, Lee D, Schulman AH. Java web tools for PCR, in silico PCR, and oligonucleotide assembly and analysis. Genomics 2011;98:137-44.
DOI: https://doi.org/10.1016/j.ygeno.2011.04.009
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 Microbiological Methods 2012;88:98-102.
DOI: https://doi.org/10.1016/j.mimet.2011.10.017
Ceccarelli D, Spagnoletti M, Bacciu D, et al. New V. cholerae atypical El Tor variant emerged during the 2006 epidemic outbreak in Angola. BMC Microbiol 2011;11:1-8.
DOI: https://doi.org/10.1186/1471-2180-11-130
Maugeri TL, Carbone M, Fera MT, Gugliandolo C. Detection and differentiation of Vibrio vulnificus in seawater and plankton of a coastal zone of the Mediterranean Sea. Res Microbiol 2006;157:194-200.
DOI: https://doi.org/10.1016/j.resmic.2005.06.007
Hammer Ø, Harper DAT, Ryan, PD. PAST-palaeontological statistics, ver. 1.89. Palaeontol Electron 2001;4:1-9.
Igere BE, Okoh AI, Nwodo UU. Antibiotic susceptibility testing (AST) reports: a basis for environmental/epidemiological surveillance and infection control amongst environmental Vibrio cholerae. Inter J Environ Res Pub Health 2020;17:5685.
DOI: https://doi.org/10.3390/ijerph17165685
Igere BE, Okoh AI, Nwodo UU. Lethality of resistant/virulent environmental Vibrio cholerae in wastewater release: an evidence of emerging virulent/antibiotic-resistant-bacteria contaminants of public health concern. EnvironChall2022;7;100504.
DOI: https://doi.org/10.1016/j.envc.2022.100504
Wozniak RA, Fouts DE, Spagnoletti M, et al. Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genetics 2009;24:e1000786.
DOI: https://doi.org/10.1371/journal.pgen.1000786
Ceccarelli D, Spagnoletti M, Bacciu D, et al. ICEVchInd5 is prevalent in epidemic Vibrio cholerae O1 El Tor strains isolated in India. Inter J Med Microbiol 2011;301:318-24.
DOI: https://doi.org/10.1016/j.ijmm.2010.11.005
Ceccarelli D, Spagnoletti M, Cappuccinelli P, et al. Origin of Vibrio cholerae in Haiti. Lancet Infect Dis 2011;11:262.
DOI: https://doi.org/10.1016/S1473-3099(11)70078-0
Chun J, Grim CJ, Hasan NA, et al. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci 2009;106:15442-7.
DOI: https://doi.org/10.1073/pnas.0907787106
Faruque SM, Tam VC, Chowdhury N, et al. Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origin of El Tor strains carrying classical CTX prophage. Proc Natl Acad Sci 2007;104:5151-6.
DOI: https://doi.org/10.1073/pnas.0700365104
Hassan F, Kamruzzaman M, Mekalanos JJ, Faruque SM. Satellite phage TLCφ enables toxigenic conversion by CTX phage through dif site alteration. Nature 2010;467:982-5.
DOI: https://doi.org/10.1038/nature09469
Tang M, Chen Q, Zhong H, et al. Exploring diversity patterns and driving mechanisms of the antibiotic resistome and microbiome in saline groundwater. J Haz Mat 2023;6:130734.
DOI: https://doi.org/10.1016/j.jhazmat.2023.130734
Mikalsen T, Pedersen T, Willems R, et al. Investigating the mobilome in clinically important lineages of Enterococcus faecium and Enterococcus faecalis. BMC Genomics 2015;16:1-6.
DOI: https://doi.org/10.1186/s12864-015-1407-6
Siefert JL. Defining the mobilome. Methods Mol Biol 2009;532:13-27.
DOI: https://doi.org/10.1007/978-1-60327-853-9_2
Deshpande AS, Fahrenfeld NL. Influence of DNA from non-viable sources on the riverine water and biofilm microbiome, resistome, mobilome, and resistance gene host assignments. J Haz Mat 2023;5:130743.
DOI: https://doi.org/10.1016/j.jhazmat.2023.130743
Boyd EF, Waldor MK. Evolutionary and functional analyses of variants of the toxin-coregulated pilus protein TcpA from toxigenic Vibrio cholerae non-O1/non-O139 serogroup isolates. The GenBank accession numbers for the sequences reported in this paper are AY078355–AY078358. Microbiol 2002;148:1655-66.
DOI: https://doi.org/10.1099/00221287-148-6-1655
Faruque SM, Kamruzzaman M, Meraj IM, et al. Pathogenic potential of environmental Vibrio cholerae strains carrying genetic variants of the toxin-coregulated pilus pathogenicity island. Infect Immun 2003;71:1020-5.
DOI: https://doi.org/10.1128/IAI.71.2.1020-1025.2003
Pal A, Roy V, Dutta P, et al Genomic islands in bacterial genome evolution and speciation. In Chu D-T, Alzahrani KJ, Mani I, Singh V, eds. Microbial genomic islands in adaptation and pathogenicity; 2023: pp. 83-109. Singapore: Springer Nature Singapore.
DOI: https://doi.org/10.1007/978-981-19-9342-8_5
Cerqueira F, Matamoros V, Bayona J, Piña B. Antibiotic resistance genes distribution in microbiomes from the soil-plant-fruit continuum in commercial Lycopersicon esculentum fields under different agricultural practices. Sci Total Environ 2019;652:660-70.
DOI: https://doi.org/10.1016/j.scitotenv.2018.10.268
Dalia AB, Seed KD, Calderwood SB, Camilli A. A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae. Proc Natl Acad Sci 2015;112:10485-90.
DOI: https://doi.org/10.1073/pnas.1509097112
Burrus V. Mechanisms of stabilization of integrative and conjugative elements. Curr Opin Microbiol 2017;38:44-50.
DOI: https://doi.org/10.1016/j.mib.2017.03.014
Igere BE, Onohuean H, Oyama G. Occurrence of new delhi metallo-beta-lactamase 1 producing Enterococcusspecies in Oghara water nexus: An emerging environmental implications of resistance dynamics. Microbiol Insights 2022;15:11786361221133731.
DOI: https://doi.org/10.1177/11786361221133731
Delavat F, Miyazaki R, Carraro N, et al. The hidden life of integrative and conjugative elements. FEMS Microbiol Rev 2017;41:512-37.
DOI: https://doi.org/10.1093/femsre/fux008
Touchon M, Bobay LM, Rocha EP. The chromosomal accommodation and domestication of mobile genetic elements. Curr Opin Microbiol 2014;22:22-9.
DOI: https://doi.org/10.1016/j.mib.2014.09.010
How to Cite
Igere, B. E., & Nwodo, U. U. (2023). Genetic characterization of non-O1/non-O139 <i>Vibrio cholerae</i> mobilome: a strategy for understanding and discriminating emerging environmental bacterial strains. Journal of Biological Research - Bollettino Della Società Italiana Di Biologia Sperimentale, 96(2). https://doi.org/10.4081/jbr.2023.11202
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