Posibilities for use of whole genome sequencing (WGS) for the analysis of Streptococcus pneumoniae isolates
Authors:
S. Vohrnová 1,2
; J. Kozáková 1
Authors place of work:
Národní referenční laboratoř pro streptokokové nákazy, Oddělení bakteriálních vzdušných nákaz, Centrum epidemiologie a mikrobiologie, Státní zdravotní ústav, Praha
1; 3. lékařská fakulta Univerzity Karlovy, Praha
2
Published in the journal:
Epidemiol. Mikrobiol. Imunol. 73, 2024, č. 1, s. 30-36
Category:
doi:
https://doi.org/10.61568/emi/11-6254/20240123/136240
Summary
Streptococcus pneumoniae (pneumococcus) is a Gram-positive coccus causing both non-invasive and invasive infectious diseases. Pneumococcal diseases are vaccine preventable. Invasive pneumococcal diseases (IPD) meeting the international case definition are reported nationally and internationally and are subject to surveillance programmes in many countries, including the Czech Republic. An important part of IPD surveillance is the monitoring of causative serotypes and their frequency over time and in relation to ongoing vaccination programmes.
In the world and in the Czech Republic, whole genome sequencing (WGS) is increasingly used for pneumococci, which allows for serotyping from sequencing data, precise analysis of their genetic relationships, and the study of genes present in their genome. Whole-genome sequencing enables the generation of reliable and internationally comparable data that can be easily shared. Sequencing data are analysed using bioinformatics tools that require knowledge in the field of natural sciences with an emphasis on genetics and expertise in bioinformatics.
This publication presents some options for pneumococcal analysis, i.e., serotyping, multilocus sequence typing (MLST), ribosomal MLST (rMLST), core genome MLST (cgMLST), whole genome MLST (wgMLST), single nucleotide polymorphism (SNP) analysis, assignment to Global Pneumococcal Sequence Cluster (GPSC), and identification of virulence genes and antibiotic resistance genes. The WGS strategies and applications for Europe and WGS implementation in practice are presented.
WGS analysis of pneumococci allows for improved IPD surveillance, thanks to molecular serotyping, more detailed typing, generation of internationally comparable data, and improved evaluation of the effectiveness of vaccination programmes.
Keywords:
Streptococcus pneumoniae – whole genome sequencing – serotyping – molecular surveillance – invazive pneumococcal disease
Zdroje
- Arbique JC, Poyart C, Trieu-Cuot P, et al. Accuracy of phenotypic and genotypic testing for identification of Streptococcus pneumoniae and description of Streptococcus pseudopneumoniae sp. nov. J Clin Microbiol., 2004;42(10):4686–4696. doi: 10.1128/JCM.42.10.4686-4696.2004. PMID: 15472328; PMCID: PMC522306.
- Wasilauskas BL, Hampton KD. An analysis of Streptococcus pneumoniae identification using biochemical and serological procedures. Diagn Microbiol Infect Dis., 1984;2(4):301–307. doi: 10.1016/0732-8893(84)90061-0. PMID: 6488747.
- Kellogg JA, Bankert DA, Elder CJ, et al. Identification of Streptococcus pneumoniae revisited. J Clin Microbiol., 2001;39(9):3373– 3375. doi: 10.1128/JCM.39.9.3373-3375.2001. PMID: 11526182; PMCID: PMC88350.
- Geno KA, Gilbert GL, Song JY, et al. Pneumococcal Capsules and Their Types: Past, Present, and Future. Clin Microbiol Rev., 2015;28(3):871–899. doi: 10.1128/CMR.00024-15. Erratum in: Clin Microbiol Rev., 2020; 34(2): PMID: 26085553; PMCID: PMC4475641.
- Bentley SD, Aanensen DM, Mavroidi A, et al. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet., 2006;2(3):e31. doi: 10.1371/journal. pgen.0020031. Epub 2006 Mar 10. PMID: 16532061; PMCID: PMC1391919.
- Ganaie F, Saad JS, McGee L, et al. A New Pneumococcal Capsule Type, 10D, is the 100th Serotype and Has a Large cps Fragment from an Oral Streptococcus. mBio., 2020;11(3):e00937–20. doi: 10.1128/mBio.00937-20. PMID: 32430472; PMCID: PMC7240158.
- Global Pneumococcal Sequencing Project (GPS) | Serotypes. [online]. [cit. 2023-08-10]. Dostupné na www: https://www. pneumogen.net/gps/serotypes.html.
- De Lencastre H, Kristinsson KG, Brito-Avô A, et al. Carriage of respiratory tract pathogens and molecular epidemiology of Streptococcus pneumoniae colonization in healthy children attending day care centers in Lisbon, Portugal. Microb Drug Resist., 1999;5(1):19–29. doi: 10.1089/mdr.1999.5.19. PMID: 10332718.
- Kellner JD, Ford-Jones EL. Streptococcus pneumoniae carriage in children attending 59 Canadian child care centers. Toronto Child Care Centre Study Group. Arch Pediatr Adolesc Med., 1999;153(5):495–502. doi: 10.1001/archpedi.153.5.495. PMID:10323630.
- Tvedskov ESF, Hovmand N, Benfield T, et al. Pneumococcal carriage among children in low and lower-middle-income countries: A systematic review. Int J Infect Dis., 2022;115:1–7. doi: 10.1016/j.ijid.2021.11.021. Epub 2021 Nov 18. PMID: 34800691.
- Vančíková Z, Trojánek M, Zemličková H, et al. Pneumococcal urinary antigen positivity in healthy colonized children: is it age dependent? Wien Klin Wochenschr., 2013;125(17–18):495–500. doi: 10.1007/s00508-013-0405-4. Epub 2013 Aug 9. PMID: 23928934.
- Hussain M, Melegaro A, Pebody RG, et al. A longitudinal household study of Streptococcus pneumoniae nasopharyngeal carriage in a UK setting. Epidemiol Infect., 2005;133(5):891–898. doi: 10.1017/S0950268805004012. PMID: 16181510; PMCID: PMC2870321.
- Arguedas A, Trzciński K, O‘Brien KL, et al. Upper respiratory tract colonization with Streptococcus pneumoniae in adults. Expert Rev Vaccines., 2020;19(4):353–366. doi: 10.1080/14760584.2020.1750378. Epub 2020 Apr 17. PMID: 32237926.
- Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis., 2004;4(3):144–154. doi: 10.1016/S1473-3099(04)00938-7. PMID: 14998500.
- Simell B, Auranen K, Käyhty H, et al. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines, 2012;11(7):841–855. doi: 10.1586/erv.12.53. PMID: 22913260.
- Platt H, Omole T, Cardona J, et al. Safety, tolerability, and immunogenicity of a 21-valent pneumococcal conjugate vaccine, V116, in healthy adults: phase 1/2, randomised, double-blind, active comparator-controlled, multicentre, US-based trial. Lancet Infect Dis., 2023;23(2):233–246. doi: 10.1016/S14733099(22)00526-6. Epub 2022 Sep 15. PMID: 36116461.
- Chichili GR, Smulders R, Santos V, et al. Phase 1/2 study of a novel 24-valent pneumococcal vaccine in healthy adults aged 18 to 64 years and in older adults aged 65 to 85 years. Vaccine, 2022;40(31):4190–4198. doi: 10.1016/j.vaccine.2022.05.079. PMID: 35690500.
- Jauneikaite E, Tocheva AS, Jefferies JM, et al. Current methods for capsular typing of Streptococcus pneumoniae. J Microbiol Methods, 2015;113:41–49. doi: 10.1016/j.mimet.2015.03.006. Epub 2015 Mar 25. PMID: 25819558.
- Neufeld F. Ueber die Agglutination der Pneumokokken und uber die Theorien der Agglutination. Zeitschrift für Hygiene und Infektionskrankheiten, 1902;40:54–72. doi:10.1007/bf02140530.S2CID 1143320.
- Merrill CW, Gwaltney JM Jr., Hendley JW, et al. Rapid identification of pneumococci. Gram stain vs. the quellung reaction. N Engl J Med., 1973;288:510–512.
- Vacková Z, Klímová M, Kozáková J. Nová molekulární metoda a schéma typizace Streptococcus pneumoniae v České republice. Zprávy Epidemiologie a Mikrobiologie, 2013; 22(1):16–18.
- European Centre for Disease Prevention and Control. Surveillance of communicable diseases in the European Union – A long-term strategy: 2008–2013. Stockholm: ECDC; 2008.
- European Centre for Disease Prevention and Control. Surveillance of communicable diseases in Europe – a concept to integrate molecular typing data into EU-level surveillance. Stockholm: ECDC; 2013.
- European Centre for Disease Prevention and Control. Roadmap for integration of molecular typing into European – level surveillance and epidemic preparedness – Version 1.2, 2013. Stockholm: ECDC; 2016.
- European Centre for Disease Prevention and Control. ECDC roadmap for integration of molecular and genomic typing into European-level surveillance and epidemic preparedness – Version 2.1, 2016-19. Stockholm: ECDC; 2016.
- European Centre for Disease Prevention and Control. Expert opinion on whole genome sequencing for public health surveillance. Stockholm: ECDC; 2016.
- ECDC public health microbiology strategy 2018–2022.
- European Centre for Disease Prevention and Control. ECDC strategic framework for the integration of molecular and genomic typing into European surveillance and multi-country outbreak investigations – 2019–2021. Stockholm: ECDC; 2019.
- Tagini F, Greub G. Bacterial genome sequencing in clinical microbiology: a pathogen-oriented review. Eur J Clin Microbiol Infect Dis., 2017;36(11):2007–2020. doi: 10.1007/s10096-0173024-6. PMID: 28639162; PMCID: PMC5653721.
- Andam CP, Hanage WP. Mechanisms of genome evolution of Streptococcus. Infect Genet Evol., 2015;33:334–342. doi: 10.1016/j.meegid.2014.11.007. PMID: 25461843; PMCID: PMC4430445.
- Coffey TJ, Enright MC, Daniels M, et al. Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae. Mol Microbiol., 1998;27(1):73–83. doi: 10.1046/j.1365-2958.1998.00658.x. PMID: 9466257.
- Croucher NJ, Harris SR, Fraser C, et al. Rapid pneumococcal evolution in response to clinical interventions. Science, 2011;331(6016):430–434. doi: 10.1126/science.1198545. PMID:21273480; PMCID: PMC3648787.
- Gindreau E, López R, García P. MM1, a temperate bacteriophage of the type 23F Spanish/USA multiresistant epidemic clone of Streptococcus pneumoniae: structural analysis of the site-specific integration system. J Virol., 2000;74(17):7803–7813. doi: 10.1128/jvi.74.17.7803-7813.2000. PMID: 10933687; PMCID: PMC112310.
- Croucher NJ, Walker D, Romero P, et al. Role of conjugative elements in the evolution of the multidrug-resistant pandemic clone Streptococcus pneumoniae Spain 23F ST81. J Bacteriol., 2009;191(5):1480–1489. doi: 10.1128/JB.01343-08. PMID: 19114491; PMCID: PMC2648205.
- Everett DB, Cornick J, Denis B, et al. Genetic characterisation of Malawian pneumococci prior to the roll-out of the PCV13 vaccine using a high-throughput whole genome sequencing approach. PLoS One, 2012;7(9):e44250. doi: 10.1371/journal. pone.0044250. PMID: 22970189; PMCID: PMC3438182.
- Liyanapathirana V, Ang I, Tsang D, et al. Application of a target enrichment-based next-generation sequencing protocol for identification and sequence-based prediction of pneumococcal serotypes. BMC Microbiol., 2014;14:60. doi: 10.1186/1471-218014-60. PMID: 24612771; PMCID: PMC3984734.
- Kapatai G, Sheppard CL, Al-Shahib A, et al. Whole genome sequencing of Streptococcus pneumoniae: development, evaluation and verification of targets for serogroup and serotype prediction using an automated pipeline. PeerJ., 2016;4:e2477. doi: 10.7717/peerj.2477. PMID: 27672516; PMCID: PMC5028725.
- Epping L, van Tonder AJ, Gladstone RA, et al. SeroBA: rapid high-throughput serotyping of Streptococcus pneumoniae from whole genome sequence data. Microb Genom., 2018;4(7):e000186. doi: 10.1099/mgen.0.000186. Erratum in: Microb Genom., 2018;4(8): PMID: 29870330; PMCID: PMC6113868.
- Knight JR, Dunne EM, Mulholland EK, et al. Determining the serotype composition of mixed samples of pneumococcus using whole-genome sequencing. Microb Genom. 2021;7(1):mgen000494. doi: 10.1099/mgen.0.000494. PMID:33355528; PMCID: PMC8115901.
- Sheppard CL, Manna S, Groves N, et al. PneumoKITy: A fast, flexible, specific, and sensitive tool for Streptococcus pneumoniae serotype screening and mixed serotype detection from genome sequence data. Microb Genom., 2022;8(12):mgen000904. doi: 10.1099/mgen.0.000904. PMID: 36748701; PMCID: PMC9837567.
- Lee JT, Li X, Hyde C, et al. PfaSTer: a machine learning-powered serotype caller for Streptococcus pneumoniae genomes. Microb Genom., 2023;9(6). doi: 10.1099/mgen.0.001033. PMID: 37279053.
- Maiden MCJ, Bygraves JA, Feil E, et al. Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A, 1998;95(6):3140–3145. doi: 10.1073/pnas.95.6.3140. PMID: 9501229.
- Enright MC, Spratt BG. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology (Reading), 1998;144 (Pt 11):3049–3060. doi: 10.1099/00221287-144-11-3049. PMID: 9846740.
- Woese CR. Bacterial evolution. Microbiol Rev., 1987;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. PMID: 2439888; PMCID: PMC373105.
- Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A, 1990;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. PMID: 2112744; PMCID: PMC54159.
- Jolley KA, Bliss CM, Bennett JS, et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology, 2012;158(4):1005–1015. doi: 10.1099/mic.0.055459-0. PMID: 22282518.
- Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics, 2010;11:595. doi: 10.1186/1471-2105-11-595. PMID: 21143983; PMCID: PMC3004885.
Poděkování
Podpořeno z programového projektu Ministerstva zdravotnictví ČR s registračním číslem NU22-09-00433.
Do redakce došlo 11. 8. 2023.
Adresa pro korespondenci:
MUDr. Sandra Vohrnová
Národní referenční laboratoř pro streptokokové nákazy,
Oddělení bakteriálních vzdušných nákaz,
Centrum epidemiologie a mikrobiologie
Státní zdravotní ústav
Šrobárova 49/48 100 00 Praha 10
e-mail: sandra.vohrnova@szu.cz
Štítky
Hygiene and epidemiology Medical virology Clinical microbiologyČlánok vyšiel v časopise
Epidemiology, Microbiology, Immunology
2024 Číslo 1
Najčítanejšie v tomto čísle
- Human papillomavirus infection (HPV) and pregnancy
- Analysis of enterobiasis in the Czech Republic in 2018–2022
- Infection of respiratory syncytial viruses (RSV) in the Czech Republic – analysis of hospitalizations and deaths in 2017–2022
- Issues of risky behaviours in university students