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Volume 10, Issue 7

Genomic study of European ribotype 002/sequence type 8 Open Access

Abstract

has significant clinical importance as a leading cause of healthcare-associated infections, with symptoms ranging from mild diarrhoea to severe colitis, and possible life-threatening complications. ribotype (RT) 002, mainly associated with MLST sequence type (ST) 8, is one of the most common RTs found in humans. This study aimed at investigating the genetic characteristics of 537 genomes of ST8/RT002. To this end, we sequenced 298 . strains representing a new European genome collection, with strains from Germany, Denmark, France and Portugal. These sequences were analysed against a global dataset consisting of 1,437 ST8 genomes available through Enterobase. Our results showed close genetic relatedness among the studied ST8 genomes, a diverse array of antimicrobial resistance (AMR) genes and the presence of multiple mobile elements. Notably, the pangenome analysis revealed an open genomic structure. ST8 shows relatively low overall variation. Thus, clonal isolates were found across different One Health sectors (humans, animals, environment and food), time periods, and geographical locations, suggesting the lineage’s stability and a universal environmental source. Importantly, this stability did not hinder the acquisition of AMR genes, emphasizing the adaptability of this bacterium to different selective pressures. Although only 2.4 % (41/1,735) of the studied genomes originated from non-human sources, such as animals, food, or the environment, we identified 9 cross-sectoral core genome multilocus sequence typing (cgMLST) clusters. Our study highlights the importance of ST8 as a prominent lineage of with critical implications in the context of One Health. In addition, these findings strongly support the need for continued surveillance and investigation of non-human samples to gain a more comprehensive understanding of the epidemiology of .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Clostridioides difficile , genomes , One Health , pangenome , phylogenetic analysis , RT002 , ST8 and zoonotic pathogen
Funding
This study was supported by the:
  • Horizon 2020 Framework Programme (Award 773830)
    • Principle Award Recipient: InesDost
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2024-07-25
2025-05-17
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References

  1. Martínez-Meléndez A, Morfin-Otero R, Villarreal-Treviño L, Baines SD, Camacho-Ortíz A et al. Molecular epidemiology of predominant and emerging Clostridioides difficile ribotypes. J Microbiol Methods 2020; 175:105974 [View Article] [PubMed]
     [Google Scholar]
  2. CDC Antibiotic Resistance Threats in the United States, 2019 Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019 [View Article]
     [Google Scholar]
  3. European Centre for Disease Prevention and Control Healthcare-associated infections: Clostridium difficile infections. ECDC. Annual epidemiological report for 2016. Stockholm: ECDC; 2018
  4. Bolton D, Marcos P. The environment, farm animals and foods as sources of Clostridioides difficile infection in humans. Foods 2023; 12:1094 [View Article] [PubMed]
     [Google Scholar]
  5. Bidet P, Barbut F, Lalande V, Burghoffer B, Petit JC. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 1999; 175:261–266 [View Article] [PubMed]
     [Google Scholar]
  6. Banawas SS. Clostridium difficile Infections: a global overview of drug sensitivity and resistance mechanisms. Biomed Res Int 2018; 2018:8414257 [View Article] [PubMed]
     [Google Scholar]
  7. Lim SC, Knight DR, Riley TV. Clostridium difficile and One Health. Clin Microbiol Infect 2020; 26:857–863 [View Article] [PubMed]
     [Google Scholar]
  8. Knight DR, Riley TV. Genomic delineation of zoonotic origins of Clostridium difficile. Front Public Health 2019; 7:164 [View Article] [PubMed]
     [Google Scholar]
  9. Tickler IA, Obradovich AE, Goering RV, Fang FC, Tenover FC et al. Changes in molecular epidemiology and antimicrobial resistance profiles of Clostridioides (Clostridium) difficile strains in the United States between 2011 and 2017. Anaerobe 2019; 60:102050 [View Article] [PubMed]
     [Google Scholar]
  10. Griffiths D, Fawley W, Kachrimanidou M, Bowden R, Crook DW et al. Multilocus sequence typing of Clostridium difficile. J Clin Microbiol 2010; 48:770–778 [View Article] [PubMed]
     [Google Scholar]
  11. Zhao H, Nickle DC, Zeng Z, Law PYT, Wilcox MH et al. Global landscape of Clostridioides difficile phylogeography, antibiotic susceptibility, and toxin polymorphisms by post-hoc whole-genome sequencing from the MODIFY I/II studies. Infect Dis Ther 2021; 10:853–870 [View Article] [PubMed]
     [Google Scholar]
  12. Brajerova M, Zikova J, Krutova M. Clostridioides difficile epidemiology in the middle and the far east. Anaerobe 2022; 74:102542 [View Article] [PubMed]
     [Google Scholar]
  13. Freeman J, Vernon J, Pilling S, Morris K, Nicholson S et al. The ClosER study: results from a three-year pan-European longitudinal surveillance of antibiotic resistance among prevalent Clostridium difficile ribotypes, 2011-2014. Clin Microbiol Infect 2018; 24:724–731 [View Article] [PubMed]
     [Google Scholar]
  14. Gonzales-Luna AJ, Carlson TJ, Dotson KM, Poblete K, Costa G et al. PCR ribotypes of Clostridioides difficile across Texas from 2011 to 2018 including emergence of ribotype 255. Emerg Microbes Infect 2020; 9:341–347 [View Article] [PubMed]
     [Google Scholar]
  15. Salazar CL, Reyes C, Cienfuegos-Gallet AV, Best E, Atehortua S et al. Subtyping of Clostridium difficile PCR ribotypes 591, 106 and 002, the dominant strain types circulating in Medellin, Colombia. PLoS One 2018; 13:e0195694 [View Article] [PubMed]
     [Google Scholar]
  16. Furuya-Kanamori L, Riley TV, Paterson DL, Foster NF, Huber CA et al. Comparison of Clostridium difficile ribotypes circulating in Australian hospitals and communities. J Clin Microbiol 2017; 55:216–225 [View Article] [PubMed]
     [Google Scholar]
  17. Kullin B, Wojno J, Abratt V, Reid SJ. Toxin A-negative toxin B-positive ribotype 017 Clostridium difficile is the dominant strain type in patients with diarrhoea attending tuberculosis hospitals in Cape Town, South Africa. Eur J Clin Microbiol Infect Dis 2017; 36:163–175 [View Article] [PubMed]
     [Google Scholar]
  18. Kong KY, Kwong TNY, Chan H, Wong K, Wong SSY et al. Biological characteristics associated with virulence in Clostridioides difficile ribotype 002 in Hong Kong. Emerg Microbes Infect 2020; 9:631–638 [View Article] [PubMed]
     [Google Scholar]
  19. Cheng VCC, Yam WC, Lam OTC, Tsang JLY, Tse EYF et al. Clostridium difficile isolates with increased sporulation: emergence of PCR ribotype 002 in Hong Kong. Eur J Clin Microbiol Infect Dis 2011; 30:1371–1381 [View Article] [PubMed]
     [Google Scholar]
  20. Zidaric V, Rupnik M. Sporulation properties and antimicrobial susceptibility in endemic and rare Clostridium difficile PCR ribotypes. Anaerobe 2016; 39:183–188 [View Article] [PubMed]
     [Google Scholar]
  21. Baktash A, Corver J, Harmanus C, Smits WK, Fawley W et al. Comparison of whole-genome sequence-based methods and PCR ribotyping for subtyping of Clostridioides difficile. J Clin Microbiol 2022; 60:e0173721 [View Article] [PubMed]
     [Google Scholar]
  22. Eyre DW, Davies KA, Davis G, Fawley WN, Dingle KE et al. Two distinct patterns of Clostridium difficile diversity across Europe indicating contrasting routes of spread. Clin Infect Dis 2018; 67:1035–1044 [View Article] [PubMed]
     [Google Scholar]
  23. Yin C, Chen DS, Zhuge J, McKenna D, Sagurton J et al. Complete genome sequences of four toxigenic Clostridium difficile clinical isolates from patients of the lower Hudson Valley, New York, USA. Genome Announc 2018; 6:e01537-17 [View Article] [PubMed]
     [Google Scholar]
  24. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890
     [Google Scholar]
  25. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biology 2019; 20:257
     [Google Scholar]
  26. Low AJ, Koziol AG, Manninger PA, Blais B, Carrillo CD. ConFindr: rapid detection of intraspecies and cross-species contamination in bacterial whole-genome sequence data. PeerJ 2019; 7:e6995
     [Google Scholar]
  27. Shen W, Le S, Li Y, Hu F. SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation. PLOS ONE 2016; 11:
     [Google Scholar]
  28. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114
     [Google Scholar]
  29. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Research 2016; 44:W16–W21 [View Article]
     [Google Scholar]
  30. Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinformatics 2003; 10:13
     [Google Scholar]
  31. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic acids research 2015; 43:e15
     [Google Scholar]
  32. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455
     [Google Scholar]
  33. Ryberg M. Phylommand - a command line software package for Phylogenetics [version 1; peer review: 2 approved with reservations]. F1000Res 2016; 5: [View Article]
     [Google Scholar]
  34. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. Fast hierarchical Bayesian analysis of population structure. Nucleic acids research 2019; 47:5539–5549
     [Google Scholar]
  35. Silva M, Machado MP, Silva DN, Rossi M, Moran-Gilad J et al. chewBBACA: A complete suite for gene-by-gene schema creation and strain identification. Microb Genom 2018; 4:
     [Google Scholar]
  36. Bletz S, Janezic S, Harmsen D, Rupnik M, Mellmann A. Defining and evaluating a core genome multilocus sequence typing scheme for genome-wide typing of Clostridium difficile. J Clin Microbiol 2018; 56:e01987-17 [View Article] [PubMed]
     [Google Scholar]
  37. Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  38. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biology 2020; 21:180
     [Google Scholar]
  39. Schwengers O, Jelonek L, Dieckmann MA, Beyvers S, Blom J et al. Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb Genom 2021; 7:
     [Google Scholar]
  40. Zhao Y, Jia X, Yang J, Ling Y, Zhang Z et al. PanGP: a tool for quickly analyzing bacterial pan-genome profile; 2014; 301297–1299
  41. Thomas P, Abdel-Glil MY, Subbaiyan A, Busch A, Eichhorn I et al. First comparative analysis of Clostridium septicum genomes provides insights into the taxonomy, species genetic diversity, and virulence related to gas gangrene. Front Microbiol 2021; 12:771945 [View Article] [PubMed]
     [Google Scholar]
  42. Feldgarden M, Brover V, Gonzalez-Escalona N, Frye JG, Haendiges J et al. AMRFinderPlus and the Reference Gene Catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence. Scientific reports 2021; 11:12728
     [Google Scholar]
  43. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2019; 47:D687–D692 [View Article] [PubMed]
     [Google Scholar]
  44. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article] [PubMed]
     [Google Scholar]
  45. Didelot X, Eyre DW, Cule M, Ip CLC, Ansari MA et al. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol 2012; 13:R118 [View Article] [PubMed]
     [Google Scholar]
  46. Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 2013; 369:1195–1205 [View Article] [PubMed]
     [Google Scholar]
  47. Tettelin H, Riley D, Cattuto C, Medini D. Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 2008; 11:472–477 [View Article] [PubMed]
     [Google Scholar]
  48. Zhao Y, Jia X, Yang J, Ling Y, Zhang Z et al. PanGP: a tool for quickly analyzing bacterial pan-genome profile. Bioinformatics 2014; 30:1297–1299 [View Article] [PubMed]
     [Google Scholar]
  49. Knight DR, Squire MM, Collins DA, Riley TV. Genome analysis of Clostridium difficile PCR ribotype 014 lineage in Australian pigs and humans reveals a diverse genetic repertoire and signatures of long-range interspecies transmission. Front Microbiol 2016; 7:2138 [View Article] [PubMed]
     [Google Scholar]
  50. Kovacs-Simon A, Leuzzi R, Kasendra M, Minton N, Titball RW et al. Lipoprotein CD0873 is a novel adhesin of Clostridium difficile. J Infect Dis 2014; 210:274–284 [View Article] [PubMed]
     [Google Scholar]
  51. Arato V, Gasperini G, Giusti F, Ferlenghi I, Scarselli M et al. Dual role of the colonization factor CD2831 in Clostridium difficile pathogenesis. Sci Rep 2019; 9:5554 [View Article] [PubMed]
     [Google Scholar]
  52. Barketi-Klai A, Hoys S, Lambert-Bordes S, Collignon A, Kansau I. Role of fibronectin-binding protein A in Clostridium difficile intestinal colonization. J Med Microbiol 2011; 60:1155–1161 [View Article] [PubMed]
     [Google Scholar]
  53. Hennequin C, Porcheray F, Waligora-Dupriet A, Collignon A, Barc M et al. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 2001; 147:87–96 [View Article] [PubMed]
     [Google Scholar]
  54. Hensbergen PJ, Klychnikov OI, Bakker D, Dragan I, Kelly ML et al. Clostridium difficile secreted Pro-Pro endopeptidase PPEP-1 (ZMP1/CD2830) modulates adhesion through cleavage of the collagen binding protein CD2831. FEBS Lett 2015; 589:3952–3958 [View Article] [PubMed]
     [Google Scholar]
  55. Pantaléon V, Soavelomandroso AP, Bouttier S, Briandet R, Roxas B et al. The Clostridium difficile protease Cwp84 modulates both biofilm formation and cell-surface properties. PLoS One 2015; 10:e0124971 [View Article] [PubMed]
     [Google Scholar]
  56. Tulli L, Marchi S, Petracca R, Shaw HA, Fairweather NF et al. CbpA: a novel surface exposed adhesin of Clostridium difficile targeting human collagen. Cell Microbiol 2013; 15:1674–1687 [View Article] [PubMed]
     [Google Scholar]
  57. Dawson LF, Peltier J, Hall CL, Harrison MA, Derakhshan M et al. Extracellular DNA, cell surface proteins and c-di-GMP promote biofilm formation in Clostridioides difficile. Sci Rep 2021; 11:3244 [View Article] [PubMed]
     [Google Scholar]
  58. Stubbs S, Rupnik M, Gibert M, Brazier J, Duerden B et al. Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett 2000; 186:307–312 [View Article] [PubMed]
     [Google Scholar]
  59. O’Grady K, Knight DR, Riley TV. Antimicrobial resistance in Clostridioides difficile. Eur J Clin Microbiol Infect Dis 2021; 40:2459–2478 [View Article] [PubMed]
     [Google Scholar]
  60. Stogios PJ, Savchenko A. Molecular mechanisms of vancomycin resistance. Protein Sci 2020; 29:654–669 [View Article] [PubMed]
     [Google Scholar]
  61. Jung Y-H, Shin ES, Kim O, Yoo JS, Lee KM et al. Characterization of two newly identified genes, vgaD and vatH, [corrected] conferring resistance to streptogramin A in Enterococcus faecium. Antimicrob Agents Chemother 2010; 54:4744–4749 [View Article] [PubMed]
     [Google Scholar]
  62. Imwattana K, Rodríguez C, Riley TV, Knight DR. A species-wide genetic atlas of antimicrobial resistance in Clostridioides difficile. Microb Genom 2021; 7:11 [View Article] [PubMed]
     [Google Scholar]
  63. Muñoz M, Restrepo-Montoya D, Kumar N, Iraola G, Camargo M et al. Integrated genomic epidemiology and phenotypic profiling of Clostridium difficile across intra-hospital and community populations in Colombia. Sci Rep 2019; 9:11293 [View Article] [PubMed]
     [Google Scholar]
  64. Pecora N, Holzbauer S, Wang X, Gu Y, Taffner S et al. Genomic analysis of Clostridioides difficile in 2 regions of the United States reveals a diversity of strains and limited transmission. J Infect Dis 2022; 225:121–129 [View Article] [PubMed]
     [Google Scholar]
  65. Senoh M, Kato H. Molecular epidemiology of endemic Clostridioides difficile infection in Japan. Anaerobe 2022; 74:102510 [View Article] [PubMed]
     [Google Scholar]
  66. Krutova M, Matejkova J, Drevinek P, Kuijper EJ, Nyc O et al. Increasing incidence of Clostridium difficile ribotype 001 associated with severe course of the infection and previous fluoroquinolone use in the Czech Republic, 2015. Eur J Clin Microbiol Infect Dis 2017; 36:2251–2258 [View Article] [PubMed]
     [Google Scholar]
  67. Bandelj P, Blagus R, Briski F, Frlic O, Vergles Rataj A et al. Identification of risk factors influencing Clostridium difficile prevalence in middle-size dairy farms. Vet Res 2016; 47:41 [View Article] [PubMed]
     [Google Scholar]
  68. Pasquale V, Romano V, Rupnik M, Capuano F, Bove D et al. Occurrence of toxigenic Clostridium difficile in edible bivalve molluscs. Food Microbiol 2012; 31:309–312 [View Article] [PubMed]
     [Google Scholar]
  69. Himsworth CG, Patrick DM, Mak S, Jardine CM, Tang P et al. Carriage of Clostridium difficile by wild urban Norway rats (Rattus norvegicus) and black rats (Rattus rattus). Appl Environ Microbiol 2014; 80:1299–1305 [View Article] [PubMed]
     [Google Scholar]
  70. Burt SA, Meijer K, Burggraaff P, Kamerich WS, Harmanus C. Wild mice in and around the city of Utrecht, the Netherlands, are carriers of Clostridium difficile but not ESBL-producing Enterobacteriaceae, Salmonella spp. or MRSA. Lett Appl Microbiol 2018; 67:513–519 [View Article] [PubMed]
     [Google Scholar]
  71. Janezic S, Ocepek M, Zidaric V, Rupnik M. Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates. BMC Microbiol 2012; 12:48 [View Article] [PubMed]
     [Google Scholar]
  72. Knight DR, Kullin B, Androga GO, Barbut F, Eckert C et al. Evolutionary and genomic insights into Clostridioides difficile sequence type 11: a diverse zoonotic and antimicrobial-resistant lineage of global One Health importance. mBio 2019; 10:e00446-19 [View Article] [PubMed]
     [Google Scholar]
  73. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
     [Google Scholar]
  74. Knight DR, Imwattana K, Kullin B, Guerrero-Araya E, Paredes-Sabja D et al. Major genetic discontinuity and novel toxigenic species in Clostridioides difficile taxonomy. eLife 2021; 10:e64325 [View Article] [PubMed]
     [Google Scholar]
  75. Golchha NC, Nighojkar A, Nighojkar S. Redefining genomic view of Clostridioides difficile through pangenome analysis and identification of drug targets from its core genome. Drug Target Insights 2022; 16:17–24 [View Article] [PubMed]
     [Google Scholar]
  76. Buddle JE, Fagan RP. Pathogenicity and virulence of Clostridioides difficile. Virulence 2023; 14:2150452 [View Article] [PubMed]
     [Google Scholar]
  77. Péchiné S, Hennequin C, Boursier C, Hoys S, Collignon A. Immunization using GroEL decreases Clostridium difficile intestinal colonization. PLoS One 2013; 8:e81112 [View Article] [PubMed]
     [Google Scholar]
  78. Bradshaw WJ, Bruxelle J-F, Kovacs-Simon A, Harmer NJ, Janoir C et al. Molecular features of lipoprotein CD0873: a potential vaccine against the human pathogen Clostridioides difficile. J Biol Chem 2019; 294:15850–15861 [View Article] [PubMed]
     [Google Scholar]
  79. Wong SH, Ip M, Hawkey PM, Lo N, Hardy K et al. High morbidity and mortality of Clostridium difficile infection and its associations with ribotype 002 in Hong Kong. J Infect 2016; 73:115–122 [View Article] [PubMed]
     [Google Scholar]
  80. Stevenson EC, Major GA, Spiller RC, Kuehne SA, Minton NP. Coinfection and emergence of rifamycin resistance during a recurrent Clostridium difficile infection. J Clin Microbiol 2016; 54:2689–2694 [View Article] [PubMed]
     [Google Scholar]
  81. Persson S, Nielsen HL, Coia JE, Engberg J, Olesen BS et al. Sentinel surveillance and epidemiology of Clostridioides difficile in Denmark, 2016 to 2019. Euro Surveill 2022; 27:49 [View Article] [PubMed]
     [Google Scholar]
  82. Indra A, Schmid D, Huhulescu S, Simons E, Hell M et al. Clostridium difficile ribotypes in Austria: a multicenter, hospital-based survey. Wien Klin Wochenschr 2015; 127:587–593 [View Article] [PubMed]
     [Google Scholar]
  83. Wang B, Lv Z, Zhang P, Su J. Molecular epidemiology and antimicrobial susceptibility of human Clostridium difficile isolates from a single institution in Northern China. Medicine 2018; 97:e11219 [View Article] [PubMed]
     [Google Scholar]
  84. Liu J, Peng L, Su H, Tang H, Chen D et al. Chromosome and plasmid features of two ST37 Clostridioides difficile strains isolated in China reveal distinct multidrug resistance and virulence determinants. Microb Drug Resist 2020; 26:1503–1508 [View Article] [PubMed]
     [Google Scholar]
  85. Frost LS, Leplae R, Summers AO, Toussaint A. Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 2005; 3:722–732 [View Article] [PubMed]
     [Google Scholar]
  86. Hargreaves KR, Clokie MRJ. A taxonomic review of Clostridium difficile phages and proposal of a novel genus, “Phimmp04likevirus”. Viruses 2015; 7:2534–2541 [View Article] [PubMed]
     [Google Scholar]
  87. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N et al. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 2006; 38:779–786 [View Article] [PubMed]
     [Google Scholar]
  88. Amy J, Johanesen P, Lyras D. Extrachromosomal and integrated genetic elements in Clostridium difficile. Plasmid 2015; 80:97–110 [View Article] [PubMed]
     [Google Scholar]
  89. Lew T, Putsathit P, Sohn KM, Wu Y, Ouchi K et al. Antimicrobial susceptibilities of Clostridium difficile Isolates from 12 Asia-Pacific countries in 2014 and 2015. Antimicrob Agents Chemother 2020; 64:e00296-20 [View Article] [PubMed]
     [Google Scholar]
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Genomic study of European Clostridioides difficile ribotype 002/sequence type 8
M Gen 10, 001270 (2024); https://doi.org/10.1099/mgen.0.001270
/content/journal/mgen/10.1099/mgen.0.001270
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