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Toxins2025; 17(1); 20; doi: 10.3390/toxins17010020

Characterisation of Staphylococcus aureus Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes lukP/Q.

Abstract: Leukocidins of Staphylococcus (S.) aureus are bicomponent toxins that form polymeric pores in host leukocyte membranes, leading to cell death and/or triggering apoptosis. Some of these toxin genes are located on prophages and are associated with specific hosts. The genes lukP/Q have been described from equine S. aureus isolates. We examined the genomes, including the lukP/Q prophages, of S. aureus strains belonging to clonal complexes CC1, CC350, CC816, and CC8115. In addition to sequencing, phages were characterised by mitomycin C induction and transmission electron microscopy (TEM). All lukP/Q prophages integrated into the lip2=geh gene, and all included also the gene scn-eq encoding an equine staphylococcal complement inhibitor. The lukP/Q prophages clustered, based on gene content and allelic variants, into three groups. One was found in CC1 and CC97 sequences; one was present mainly in CC350 but also in other lineages (CC1, CC97, CC133, CC398); and a third one was exclusively observed in CC816 and CC8115. Prophages of the latter group additionally included a rare enterotoxin A allele (sea320E). Moreover, a prophage from a CC522 goat isolate was found to harbour lukP. Its lukF component could be regarded as chimaera comprising parts of lukQ and of lukF-P83. A putative kinase gene of 1095 basepairs was found to be associated with equine strains of S. aureus. It was also localised on prophages. However, these prophages were different from the ones that carried lukP/Q, and three different integration sites of kinase-carrying phages were identified. These observations confirmed the presence of prophage-located important virulence-associated genes in equine S. aureus and that certain prophages might determine the host specificity of the staphylococcal strains they reside in.
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Publication Date: 2025-01-03 PubMed ID: 39852974PubMed Central: PMC11769447DOI: 10.3390/toxins17010020Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study analyzed Staphylococcus aureus from horses (and some other animals) to identify which embedded viruses (prophages) carry horse-targeted white-blood-cell toxins and how these viruses shape the bacteria’s host preference. The authors show that specific prophages consistently carry equine-adapted immune-evasion genes and insert at the same genomic site, forming distinct groups linked to particular bacterial lineages.

What problem the study addressed and why it matters

  • Staphylococcus aureus produces leukocidins—two-part toxins that punch holes in host immune cells—contributing to disease and host adaptation.
  • Some leukocidin genes sit on prophages (bacterial viruses integrated into the genome) that can move between strains and influence which host species a strain infects best.
  • The leukocidin genes lukP/Q have been reported mainly in equine isolates, but their genomic context, diversity, and relationship to host specificity had not been comprehensively defined.
  • Clarifying which prophages carry lukP/Q, where they integrate, and which other virulence genes they transport can reveal how S. aureus adapts to horses and potentially crosses species.

What the researchers did

  • Collected S. aureus strains from several clonal complexes (CCs): CC1, CC350, CC816, and CC8115, with additional comparative observations across CC97, CC133, CC398, and a CC522 goat isolate.
  • Sequenced bacterial genomes to identify prophages, their integration sites, and gene cargo, focusing on lukP/Q and related virulence genes.
  • Induced prophages with mitomycin C to confirm inducibility and examined phage particles using transmission electron microscopy (TEM).
  • Clustered lukP/Q-carrying prophages based on gene content and allelic variants to define groups and their association with bacterial lineages.

Key findings

  • Consistent integration site: All lukP/Q prophages integrated into the lip2=geh locus (a lipase gene), indicating a conserved attachment site across diverse strains.
  • Shared immune-evasion cargo: Every lukP/Q prophage also carried scn-eq, an equine staphylococcal complement inhibitor, reinforcing equine host adaptation.
  • Three prophage groups:
    • Group 1: Found in CC1 and CC97 sequences.
    • Group 2: Predominantly in CC350, but also present in CC1, CC97, CC133, and CC398.
    • Group 3: Restricted to CC816 and CC8115 (equine-associated lineages).
  • Additional virulence gene in Group 3: Prophages in CC816/CC8115 carried a rare enterotoxin A allele (sea320E), highlighting lineage-specific toxin complements.
  • Chimeric leukocidin in a goat isolate: A prophage from a CC522 goat strain carried lukP, and its lukF component was a chimera composed of parts of lukQ and lukF-P83, indicating recombination-driven toxin diversification.
  • Equine-associated kinase gene: A 1095-bp putative kinase gene was linked to equine strains and located on prophages distinct from lukP/Q carriers; these kinase phages integrated at three different genomic sites.
  • Overall implication: Important virulence factors in equine S. aureus reside on prophages, and specific prophages likely contribute to host specificity.

How to interpret these results

  • Host adaptation via phage cargo: The co-location of lukP/Q with scn-eq on prophages suggests a coordinated package of toxins and immune modulators tuned to the equine immune system, promoting horse-specific fitness.
  • Conserved integration at lip2=geh: Repeated targeting of the lip2=geh locus implies either a favored phage attachment site or potential advantages from disrupting/modulating this region; either scenario supports stable maintenance of virulence cargo.
  • Lineage–phage matching: The three prophage groups map onto specific clonal complexes, indicating that both bacterial lineage and phage type co-evolve to shape toxin repertoires and host range.
  • Recombination and mosaic toxins: The chimeric lukF in the goat isolate exemplifies how phage-borne leukocidins can recombine, potentially altering cell specificity and potency and enabling spillover between hosts.
  • Parallel phage systems: The equine-associated kinase gene being carried by different prophages and integrating at multiple sites shows that more than one phage system contributes to virulence and host adaptation in equine strains.

Methods insight and why they matter

  • Whole-genome sequencing provided high-resolution maps of prophage insertion sites and gene cassettes, enabling accurate grouping of lukP/Q phages by content and alleles.
  • Mitomycin C induction confirmed that the prophages are active (capable of entering the lytic cycle), which is relevant for horizontal gene transfer and outbreak dynamics.
  • TEM established the presence and morphology of induced phage particles, corroborating genomic predictions with direct visualization.

Implications for surveillance and control

  • Molecular markers for equine S. aureus: The combination of lukP/Q, scn-eq, and integration at lip2=geh offers a practical genomic signature to identify horse-adapted strains.
  • Risk of cross-species transfer: Detection of lukP-related genes in non-equine lineages (e.g., CC522 goat, CC398) underscores the potential for interspecies movement of virulence factors via prophages.
  • Targeted monitoring: Veterinary diagnostics and One Health surveillance can track specific prophage groups to anticipate emergence and spread of equine-adapted S. aureus.
  • Therapeutic considerations: Understanding prophage cargo and stability may inform strategies that avoid inadvertently inducing prophages (which could mobilize toxins) and guide vaccine or antitoxin design focused on equine-specific leukocidins.

Limitations and future directions

  • Sampling breadth: While multiple clonal complexes were assessed, the abstract does not specify sample sizes per lineage; broader geographic and host sampling would strengthen generalizability.
  • Functional assays: The study maps genes and phage groups but does not detail comparative toxin activity or host-cell targeting across prophage types; future work could test cytotoxicity and immune evasion in vitro and in vivo.
  • Evolutionary dynamics: Longitudinal studies could clarify how frequently lukP/Q prophages move between lineages and what ecological pressures favor integration at lip2=geh.
  • Clinical correlation: Linking prophage types to clinical outcomes in horses (e.g., disease severity, tissue tropism) would translate genomic signatures into prognostic or therapeutic value.

Cite This Article

APA
Monecke S, Burgold-Voigt S, Feßler AT, Krapf M, Loncaric I, Liebler-Tenorio EM, Braun SD, Diezel C, Müller E, Reinicke M, Reissig A, Cabal Rosel A, Ruppitsch W, Hotzel H, Hanke D, Cuny C, Witte W, Schwarz S, Ehricht R. (2025). Characterisation of Staphylococcus aureus Strains and Their Prophages That Carry Horse-Specific Leukocidin Genes lukP/Q. Toxins (Basel), 17(1), 20. https://doi.org/10.3390/toxins17010020

Publication

Toxins
ISSN: 2072-6651
NlmUniqueID: 101530765
Country: Switzerland
Language: English
Volume: 17
Issue: 1
PII: 20

Researcher Affiliations

Monecke, Stefan
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Burgold-Voigt, Sindy
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Feßler, Andrea T
  • Institute of Microbiology and Epizootics and Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany.
Krapf, Martina
  • LABOKLIN GmbH&Co. KG, 97688 Bad Kissingen, Germany.
Loncaric, Igor
  • Institute of Microbiology, University of Veterinary Medicine Vienna, 1210 Vienna, Austria.
Liebler-Tenorio, Elisabeth M
  • Institute of Molecular Pathogenesis, Friedrich-Loeffler-Institute (Federal Research Institute for Animal Health), 07743 Jena, Germany.
Braun, Sascha D
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Diezel, Celia
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Müller, Elke
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Reinicke, Martin
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Reissig, Annett
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
Cabal Rosel, Adriana
  • Austrian Agency for Health and Food Safety (AGES), Institute for Medical Microbiology and Hygiene, 1090 Vienna, Austria.
Ruppitsch, Werner
  • Austrian Agency for Health and Food Safety (AGES), Institute for Medical Microbiology and Hygiene, 1090 Vienna, Austria.
  • FoodHub-Centre of Excellence for Digitalisation of Microbial Food Safety Risk Assessment and Quality Parameters for AccurFood Authenticity Certification, University of Donja Gorica, 81000 Podgorica, Montenegro.
Hotzel, Helmut
  • Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institute (Federal Research Institute for Animal Health), 07743 Jena, Germany.
Hanke, Dennis
  • Institute of Microbiology and Epizootics and Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany.
Cuny, Christiane
  • Robert Koch Institute, Wernigerode Branch, 38855 Wernigerode, Germany.
Witte, Wolfgang
  • Robert Koch Institute, Wernigerode Branch, 38855 Wernigerode, Germany.
Schwarz, Stefan
  • Institute of Microbiology and Epizootics and Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany.
Ehricht, Ralf
  • Leibniz Institute of Photonic Technology (Leibniz-IPHT), Leibniz Center for Photonics in Infection Research (LPI), Germany and InfectoGnostics Research Campus, 07745 Jena, Germany.
  • Institute of Physical Chemistry, Friedrich-Schiller University, 07743 Jena, Germany.

MeSH Terms

  • Horses / microbiology
  • Prophages / genetics
  • Prophages / ultrastructure
  • Animals
  • Staphylococcus aureus / genetics
  • Staphylococcus aureus / virology
  • Leukocidins / genetics
  • Bacterial Proteins / genetics
  • Staphylococcal Infections / veterinary
  • Staphylococcal Infections / microbiology

Grant Funding

  • 13GW0456 / Federal Ministry of Education and Research
  • 13N15717 / Federal Ministry of Education and Research

Conflict of Interest Statement

Martina Krapf is employed by the veterinary laboratory provider LABOKLIN GmbH&Co. KG. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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