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PloS one2025; 20(11); e0333701; doi: 10.1371/journal.pone.0333701

Genomic epidemiology of strains currently and formerly classified as Enterobacter spp. recovered from equine necropsy samples.

Abstract: Enterobacteriaceae are opportunistic pathogens responsible for local or systemic infections in both human and veterinary medicine. To monitor circulating strains in stud farms in Normandy (France), we investigated a collection of Enterobacteriaceae isolated from necropsied equids performed in the region between 1997 and 2020. These strains were initially identified using MALDI-TOF; however, as this method failed to identify some isolates, whole genome sequencing followed by rMLST analysis was subsequently performed. Different genera were identified: Enterobacter spp., Huaxiibacter spp., Lelliottia spp., Rahnella spp.. MALDI-TOF and rMLST identifications were concordant for only 26.5% of the strains studied, leading us to conclude that rMLST is a more reliable method for both genus- and species-level identification, particularly for less-studied genera such as Huaxiibacter spp. and Rahnella spp.. The genus Enterobacter spp. (E. hormaechei and E. ludwigii) accounted for 53% of the strains with a high degree of sequence type (ST) diversity. These include E. hormaechei ST114 and ST171, known as high-risk clone in human clinical medicine. These clones, containing plasmids and acquired resistance genes such as blaOXA-1, blaSHV-12 or blaTEM-1B, are resistant to at least four classes of antibiotics. The presence of genes encoding the enteroaggregative heat-stable enterotoxin 1 or the bacteriocin colicin, probably carried by plasmids, implies that Enterobacter spp. form a reservoir of antibiotic resistance and virulence factors. Conversely, strains of the genera Huaxiibacter spp., Lelliottia spp. and Rahnella spp. naturally found in the environment, showed a lean resistome and virulome. This analysis shows that genomic studies are essential to obtain precise species identification, monitor and detect high-risk clones, and to highlight the circulation of resistance and virulence genes through mobile genetic elements.
Publication Date: 2025-11-13 PubMed ID: 41231827PubMed Central: PMC12614608DOI: 10.1371/journal.pone.0333701Google Scholar: Lookup
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  • Journal Article

Summary

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Overview

  • This study analyzed bacterial strains isolated from horse necropsy samples in Normandy, France, originally classified as Enterobacter spp.
  • Using whole genome sequencing and ribosomal multilocus sequence typing (rMLST), the research reclassified these strains, assessed antibiotic resistance, and identified virulence factors, highlighting the importance of genomic tools in veterinary pathogen surveillance.

Background and Purpose

  • Enterobacteriaceae are a family of bacteria that can cause opportunistic infections in humans and animals.
  • Monitoring bacterial strains from stud farms is crucial for understanding infectious risks and managing treatment strategies in veterinary settings.
  • MALDI-TOF, a common bacterial identification tool, sometimes fails to accurately identify environmental or less-studied strains.
  • The study aimed to improve identification accuracy for Enterobacteriaceae isolates from equine necropsy samples collected over more than two decades (1997–2020) in Normandy, France.

Methods

  • Initial bacterial identification was performed using MALDI-TOF mass spectrometry.
  • For strains that MALDI-TOF failed to identify confidently, whole genome sequencing (WGS) was performed.
  • rMLST analysis, a genetic sequencing approach targeting ribosomal gene loci, was used for genus and species determination after WGS.
  • Comparisons between MALDI-TOF and rMLST identifications were made to evaluate accuracy and concordance.
  • Genomic analysis included screening for antibiotic resistance genes, virulence factors like enterotoxins and bacteriocins, and plasmids (mobile genetic elements facilitating gene transfer).

Key Findings

  • The strains originally classified as Enterobacter spp. were actually from multiple genera:
    • Enterobacter spp. (including E. hormaechei and E. ludwigii)
    • Huaxiibacter spp.
    • Lelliottia spp.
    • Rahnella spp.
  • Only about 26.5% of strain identifications matched between MALDI-TOF and rMLST, indicating MALDI-TOF’s limitations for some genera.
  • rMLST was considered more reliable for accurate genus and species classification, especially for under-studied genera like Huaxiibacter and Rahnella.

Genetic Diversity and Resistance

  • 53% of strains were confirmed as Enterobacter spp., showing high sequence type diversity.
  • Notably, high-risk Enterobacter clones known from human medicine were detected:
    • E. hormaechei ST114
    • E. hormaechei ST171
  • These clones carried plasmids with acquired antibiotic resistance genes such as:
    • blaOXA-1
    • blaSHV-12
    • blaTEM-1B
  • These genes confer resistance to at least four antibiotic classes, highlighting multidrug resistance.

Virulence Factors

  • Some Enterobacter strains contained genes encoding:
    • Enteroaggregative heat-stable enterotoxin 1 (a toxin linked with pathogenicity)
    • Bacteriocin colicin (a protein that can kill competing bacteria)
  • These virulence factors are probably plasmid-encoded, meaning they can spread between bacteria.
  • This suggests Enterobacter spp. in horses may act as reservoirs for both antibiotic resistance and virulence genes.

Environmental Genera Characteristics

  • Strains from Huaxiibacter, Lelliottia, and Rahnella genera were found to be naturally environmental bacteria.
  • These genera showed minimal antibiotic resistance genes (lean resistome) and few virulence factors (lean virulome).
  • This supports their lesser role as opportunistic pathogens compared to Enterobacter spp.

Conclusions and Implications

  • Genomic studies like WGS and rMLST are essential for:
    • Precise bacterial species identification beyond traditional methods like MALDI-TOF.
    • Monitoring emerging and high-risk clones that pose risks in veterinary and potentially human contexts.
    • Tracking dissemination of antibiotic resistance and virulence genes, particularly via plasmids and mobile genetic elements.
  • This study highlights a potential reservoir of multidrug-resistant and virulent Enterobacter strains in equine populations.
  • Veterinary microbiology should adopt genomic surveillance to inform infection control, antibiotic stewardship, and disease management strategies in animal farms.

Cite This Article

APA
Harel B, Sévin C, Le Hello S, Moreau P, Giard JC, Petry S, Gravey F. (2025). Genomic epidemiology of strains currently and formerly classified as Enterobacter spp. recovered from equine necropsy samples. PLoS One, 20(11), e0333701. https://doi.org/10.1371/journal.pone.0333701

Publication

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 20
Issue: 11
Pages: e0333701
PII: e0333701

Researcher Affiliations

Harel, Blandine
  • Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, F-14000 Caen, France.
Sévin, Corinne
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
Le Hello, Simon
  • Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, F-14000 Caen, France.
  • Department of Infectious Agents, Bacteriology, CHU Caen, F-14000 Caen, France.
Moreau, Peggy
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
Giard, Jean-Christophe
  • Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, F-14000 Caen, France.
Petry, Sandrine
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
Gravey, François
  • Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, F-14000 Caen, France.
  • Department of Infectious Agents, Bacteriology, CHU Caen, F-14000 Caen, France.

MeSH Terms

  • Animals
  • Horses / microbiology
  • Enterobacter / genetics
  • Enterobacter / isolation & purification
  • Enterobacter / classification
  • Enterobacteriaceae Infections / epidemiology
  • Enterobacteriaceae Infections / microbiology
  • Enterobacteriaceae Infections / veterinary
  • Horse Diseases / microbiology
  • Horse Diseases / epidemiology
  • Whole Genome Sequencing
  • Genome, Bacterial
  • Phylogeny
  • Anti-Bacterial Agents / pharmacology
  • France / epidemiology
  • Genomics
  • Autopsy
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Microbial Sensitivity Tests

Conflict of Interest Statement

The authors have declared that no competing interests exist.

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