Skip to content
1887

Microbial Genomics logo Microbial Genomics

Volume 11, Issue 4

Whole-genome-based characterization of strains isolated from paediatric diarrhoeal cases in Kolkata, India Open Access

Abstract

is a Gram-negative facultative anaerobic bacterium that causes diarrhoea in humans. This study shows the isolation of from hospitalized paediatric diarrhoeal cases and genome-based characteristics with putative virulence factors and antimicrobial resistance. isolates were identified by species-specific PCR, targeting the gene encoding cytolethal distending toxin (). The genome of was sequenced to identify (i) genes encoding virulence factors (ii) antibiotic resistance-encoding genes, including the mobile genetic elements and (iii) core gene-based phylogenetic relationships and pan-genome features. A total of 10 (1.2%) isolates were isolated from 854 faecal samples, of which 6 (60%) were found as the sole pathogen and the remaining 4 (40%) were identified along with other pathogens, such as enteroaggregative , rotavirus and adenovirus. Patients from whom was isolated presented cholera-like diarrhoea, i.e. with watery stool (60%) with moderate dehydration (100%), fever (20%) and abdominal pain (20%). The antimicrobial susceptibility testing of showed that most of the isolates were susceptible or reduced susceptible to most of the antibiotics except resistance to erythromycin (80%), tetracycline (50%), nalidixic acid (40%), ampicillin (40%), doxycycline (30%) and ceftriaxone (20%). In the whole-genome sequence, isolates revealed several virulence-encoding genes, namely the intimin (, attaching and effacing), the cytolethal distending toxin type II subunit A (), adhesion (, porcine attaching- and effacing-associated), non-LEE (locus of enterocyte effacement) encoded effector A () and antimicrobial resistance genes (ARGs) conferring resistance to tetracycline (, ), sulphonamides (), fluoroquinolones () and beta-lactamases ( , a). The SNP-based phylogenetic analysis of 647 whole genomes of isolates from the National Center for Biotechnology Information databases did not reveal any comparable clustering pattern based on the biological source and place of isolation. The genome of some of the was closely related to those of the isolates from China and the United Kingdom. The PFGE patterns revealed that most of the isolates were distinct clones. This study reports on the extensive genome analysis of diarrhoea-associated harbouring multiple virulence and ARGs.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial resistance , diarrhoea , E. albertii , virulence and whole-genome sequence
Funding
This study was supported by the:
  • Indian Council of Medical Research
    • Principle Award Recipient: AsishK Mukhopadhyay
  • Japan Agency for Medical Research and Development (Award JP23wm0125004 and JP23wm0225021)
    • Principle Award Recipient: Shin-ichiMiyoshi
© 2025 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001363
2025-04-08
2025-04-27
Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/4/mgen001363.html?itemId=/content/journal/mgen/10.1099/mgen.0.001363&mimeType=html&fmt=ahah

References

  1. Gomes TAT, Ooka T, Hernandes RT, Yamamoto D, Hayashi T. Escherichia albertii pathogenesis. EcoSal Plus 2020; 9: [View Article]
     [Google Scholar]
  2. Ooka T, Ogura Y, Katsura K, Seto K, Kobayashi H et al. Defining the genome features of Escherichia albertii, an emerging enteropathogen closely related to Escherichia coli. Genome Biol Evol 2015; 7:3170–3179 [View Article] [PubMed]
     [Google Scholar]
  3. Hyma KE, Lacher DW, Nelson AM, Bumbaugh AC, Janda JM et al. Evolutionary genetics of a new pathogenic Escherichia species: Escherichia albertii and related Shigella boydii strains. J Bacteriol 2005; 187:619–628 [View Article] [PubMed]
     [Google Scholar]
  4. Albert MJ, Alam K, Islam M, Montanaro J, Rahaman AS et al. Hafnia alvei, a probable cause of diarrhea in humans. Infect Immun 1991; 59:1507–1513 [View Article] [PubMed]
     [Google Scholar]
  5. Huys G, Cnockaert M, Janda JM, Swings J. Escherichia albertii sp. nov., a diarrhoeagenic species isolated from stool specimens of Bangladeshi children. Int J Syst Evol Microbiol 2003; 53:807–810 [View Article] [PubMed]
     [Google Scholar]
  6. Lima MP, Yamamoto D, Santos AC de M, Ooka T, Hernandes RT et al. Phenotypic characterization and virulence-related properties of Escherichia albertii strains isolated from children with diarrhea in Brazil. Pathog Dis 2019; 77:ftz014 [View Article] [PubMed]
     [Google Scholar]
  7. Wang H, Li Q, Bai X, Xu Y, Zhao A et al. Prevalence of eae-positive, lactose non-fermenting Escherichia albertii from retail raw meat in China. Epidemiol Infect 2016; 144:45–52 [View Article] [PubMed]
     [Google Scholar]
  8. Ooka T, Tokuoka E, Furukawa M, Nagamura T, Ogura Y et al. Human gastroenteritis outbreak associated with Escherichia albertii, Japan. Emerg Infect Dis 2013; 19:144–146 [View Article] [PubMed]
     [Google Scholar]
  9. Maldonado-Puga S, Meza-Segura M, Becerra A, Zaidi MB, Estrada-Garcia T. Draft genome sequence of Escherichia albertii strain Mex-12/320a, isolated from an infant with diarrhea and harboring virulence genes associated with diarrheagenic strains of enteropathogenic Escherichia coli. Microbiol Resour Announc 2019; 8:e00208-19 [View Article] [PubMed]
     [Google Scholar]
  10. Leszczyńska K, Święcicka I, Daniluk T, Lebensztejn D, Chmielewska-Deptuła S et al. Escherichia albertii as a potential enteropathogen in the light of epidemiological and genomic studies. Genes 2023; 14:1384 [View Article] [PubMed]
     [Google Scholar]
  11. Barmettler K, Biggel M, Treier A, Muchaamba F, Vogler BR et al. Occurrence and characteristics of Escherichia albertii in wild birds and poultry flocks in Switzerland. Microorganisms 2022; 10:2265 [View Article] [PubMed]
     [Google Scholar]
  12. Bengtsson RJ, Baker KS, Cunningham AA, Greig DR, John SK et al. The genomic epidemiology of Escherichia albertii infecting humans and birds in Great Britain. Nat Commun 2023; 14:1707 [View Article] [PubMed]
     [Google Scholar]
  13. Lindsey RL, Rowe LA, Batra D, Smith P, Strockbine NA et al. PacBio genome sequences of eight Escherichia albertii strains isolated from humans in the United States. Microbiol Resour Announc 2019; 8:e01663-18 [View Article] [PubMed]
     [Google Scholar]
  14. Liu Q, Bai X, Yang X, Fan G, Wu K et al. Identification and genomic characterization of Escherichia albertii in migratory birds from Poyang Lake, China. Pathogens 2022; 12:9 [View Article]
     [Google Scholar]
  15. Naka A, Hinenoya A, Awasthi SP, Yamasaki S. Isolation and characterization of Escherichia albertii from wild and safeguarded animals in Okayama Prefecture and its prefectural borders, Japan. J Vet Med Sci 2022; 84:1299–1306 [View Article] [PubMed]
     [Google Scholar]
  16. Hinenoya A, Wang H, Patrick EM, Zeng X, Cao L et al. Longitudinal surveillance and comparative characterization of Escherichia albertii in wild raccoons in the United States. Microbiol Res 2022; 262:127109 [View Article] [PubMed]
     [Google Scholar]
  17. Muchaamba F, Barmettler K, Treier A, Houf K, Stephan R. Microbiology and epidemiology of Escherichia albertii—an emerging elusive foodborne pathogen. Microorganisms 2022; 10:875 [View Article] [PubMed]
     [Google Scholar]
  18. Ori EL, Takagi EH, Andrade TS, Miguel BT, Cergole-Novella MC et al. Diarrhoeagenic Escherichia coli and Escherichia albertii in Brazil: pathotypes and serotypes over a 6-year period of surveillance. Epidemiol Infect 2018; 147:e10 [View Article] [PubMed]
     [Google Scholar]
  19. Masuda K, Ooka T, Akita H, Hiratsuka T, Takao S et al. Epidemiological aspects of Escherichia albertii outbreaks in Japan and genetic characteristics of the causative pathogen. Foodborne Pathog Dis 2020; 17:144–150 [View Article] [PubMed]
     [Google Scholar]
  20. Iguchi A, Takemura T, Ogura Y, Nguyen TTH, Kikuchi T et al. Genomic characterization of endemic diarrheagenic Escherichia coli and Escherichia albertii from infants with diarrhea in Vietnam. PLoS Negl Trop Dis 2023; 17:e0011259 [View Article] [PubMed]
     [Google Scholar]
  21. Foroughi A, Namdari A, Rahimian-Zarif B. Detection of Escherichia albertii in urinary and gastrointestinal infections in Kermanshah, Iran. Int J Enteric Pathog 2021; 9:37–42 [View Article]
     [Google Scholar]
  22. Maeda E, Murakami K, Sera N, Ito K, Fujimoto S. Detection of Escherichia albertii from chicken meat and giblets. J Vet Med Sci 2015; 77:871–873 [View Article] [PubMed]
     [Google Scholar]
  23. Bhatt S, Egan M, Critelli B, Kouse A, Kalman D et al. he evasive enemy: Insights into the virulence and epidemiology of the emerging attaching and effacing pathogen Escherichia albertii. Infect Immun 2019; 87:e00254-18 [View Article] [PubMed]
     [Google Scholar]
  24. Brandal LT, Tunsjø HS, Ranheim TE, Løbersli I, Lange H et al. Shiga toxin 2a in Escherichia albertii. J Clin Microbiol 2015; 53:1454–1455 [View Article] [PubMed]
     [Google Scholar]
  25. WHO Guideline: updates on the management of severe acute malnutrition in infants and children; 2013 https://www.who.int/publications/i/item/9789241506328 accessed 22 May 2021
  26. Nair GB, Ramamurthy T, Bhattacharya MK, Krishnan T, Ganguly S et al. Emerging trends in the etiology of enteric pathogens as evidenced from an active surveillance of hospitalized diarrhoeal patients in Kolkata, India. Gut Pathog 2010; 2:4 [View Article] [PubMed]
     [Google Scholar]
  27. Edwards PR, Ewing WHE. Edwards and Ewing’s Identification of Enterobacteriaceae, 4th edn New York: Elsevier; 1986 pp 7–142
     [Google Scholar]
  28. Panchalingam S, Antonio M, Hossain A, Mandomando I, Ochieng B et al. Diagnostic microbiologic methods in the GEMS-1 case/control study. Clin Infect Dis 2012; 55 Suppl 4:S294–302 [View Article] [PubMed]
     [Google Scholar]
  29. Hinenoya A, Ichimura H, Yasuda N, Harada S, Yamada K et al. Development of a specific cytolethal distending toxin (cdt) gene (Eacdt)-based PCR assay for the detection of Escherichia albertii. Diagn Microbiol Infect Dis 2019; 95:119–124 [View Article] [PubMed]
     [Google Scholar]
  30. Clinical and Laboratory Standards Institute (CLSI) CLSI supplement M100. CLSI. In Performance Standards for Antimicrobial Susceptibility Testing, 32nd Ed 2022
     [Google Scholar]
  31. Bessonov K, Laing C, Robertson J, Yong I, Ziebell K et al. ECTyper: in silico Escherichia coli serotype and species prediction from raw and assembled whole-genome sequence data. Microb Genom 2021; 7:000728 [View Article] [PubMed]
     [Google Scholar]
  32. Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB et al. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 2006; 3:59–67 [View Article] [PubMed]
     [Google Scholar]
  33. Kajitani R, Yoshimura D, Ogura Y, Gotoh Y, Hayashi T et al. Platanus_B: an accurate de novo assembler for bacterial genomes using an iterative error-removal process. DNA Res 2020; 27:dsaa014 [View Article] [PubMed]
     [Google Scholar]
  34. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  35. 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 [View Article] [PubMed]
     [Google Scholar]
  36. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  37. 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]
  38. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
     [Google Scholar]
  39. 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 [View Article] [PubMed]
     [Google Scholar]
  40. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 2013; 30:1224–1228 [View Article] [PubMed]
     [Google Scholar]
  41. 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]
  42. Arimizu Y, Kirino Y, Sato MP, Uno K, Sato T et al. Large-scale genome analysis of bovine commensal Escherichia coli reveals that bovine-adapted E. coli lineages are serving as evolutionary sources of the emergence of human intestinal pathogenic strains. Genome Res 2019; 29:1495–1505 [View Article] [PubMed]
     [Google Scholar]
  43. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58:212–220 [View Article] [PubMed]
     [Google Scholar]
  44. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article]
     [Google Scholar]
  45. 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. Sci Rep 2021; 11:12728 [View Article] [PubMed]
     [Google Scholar]
  46. Pakbin B, Brück WM, Rossen JWA. Virulence factors of enteric pathogenic Escherichia coli: A review. Int J Mol Sci 2021; 22:9922 [View Article] [PubMed]
     [Google Scholar]
  47. Ooka T, Seto K, Kawano K, Kobayashi H, Etoh Y et al. Clinical significance of Escherichia albertii. Emerg Infect Dis 2012; 18:488–492 [View Article] [PubMed]
     [Google Scholar]
  48. Asoshima N, Matsuda M, Shigemura K, Honda M, Yoshida H et al. Identification of Escherichia albertii as a causative agent of a food-borne outbreak occurred in 2003. Jpn J Infect Dis 2014; 67:139–140 [View Article] [PubMed]
     [Google Scholar]
  49. Sulaiman MA, Aminu M, Ella EE, Abdullahi IO. Prevalence and risks factors of the novel Escherichia albertii among gastroenteritis patients in Kano State, Nigeria. J Med Trop 2021; 23:39–45 [View Article]
     [Google Scholar]
  50. Bhatt S, Egan M, Ramirez J, Xander C, Upreti C. Harnessing the power of recombineering to interrogate the virulome of Escherichia albertii. Gene Transl Bioinformatics 2016; 2:1–7
     [Google Scholar]
  51. Nimri LF. Escherichia albertii, a newly emerging enteric pathogen with poorly defined properties. Diagn Microbiol Infect Dis 2013; 77:91–95 [View Article] [PubMed]
     [Google Scholar]
  52. Oaks JL, Besser TE, Walk ST, Gordon DM, Beckmen KB et al. Escherichia albertii in wild and domestic birds. Emerg Infect Dis 2010; 16:638–646 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001363
Loading
Whole-genome-based characterization of Escherichia albertii strains isolated from paediatric diarrhoeal cases in Kolkata, India
M Gen 11, 001363 (2025); https://doi.org/10.1099/mgen.0.001363
/content/journal/mgen/10.1099/mgen.0.001363
/content/journal/mgen/10.1099/mgen.0.001363
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error