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Comparative genomic analysis of Streptococcus parasuis and Streptococcus suis reveals mobile element-associated enrichment of antimicrobial resistance and lack of detectable same-MGE colocalization with virulence-associated genes within stable species boundaries.

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Τίτλος: Comparative genomic analysis of Streptococcus parasuis and Streptococcus suis reveals mobile element-associated enrichment of antimicrobial resistance and lack of detectable same-MGE colocalization with virulence-associated genes within stable species boundaries.
Συγγραφείς: Zhen Z; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China., Baihe M; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China., Meiliang G; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China., Yuxuan W; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China., Lianrui L; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China. Electronic address: 15136351829@163.com.
Πηγή: Comparative immunology, microbiology and infectious diseases [Comp Immunol Microbiol Infect Dis] 2026 Sep; Vol. 129, pp. 102519. Date of Electronic Publication: 2026 Aug 25.
Τύπος έκδοσης: Journal Article; Comparative Study
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Elsevier Science Ltd Country of Publication: England NLM ID: 7808924 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1878-1667 (Electronic) Linking ISSN: 01479571 NLM ISO Abbreviation: Comp Immunol Microbiol Infect Dis Subsets: MEDLINE
Imprint Name(s): Publication: Exeter : Elsevier Science Ltd
Original Publication: Oxford, Elmsford, N. Y., Pergamon Press.
Ιατρικοί όροι (MeSH): Streptococcus suis*/genetics , Streptococcus suis*/drug effects , Streptococcus suis*/pathogenicity , Interspersed Repetitive Sequences*/genetics , Streptococcal Infections*/microbiology , Streptococcal Infections*/veterinary , Drug Resistance, Bacterial*/genetics , Genome, Bacterial*, Virulence/genetics ; Virulence Factors/genetics ; Anti-Bacterial Agents/pharmacology ; Swine Diseases/microbiology ; Animals ; Swine ; Genomics ; Genotype ; China ; Microbial Sensitivity Tests
Περίληψη: Streptococcus suis is a major porcine pathogen and a zoonotic agent that causes meningitis and septicemia in humans. Streptococcus parasuis, a recently recognized close relative, remains poorly characterized with regard to its clinical significance and genomic features. In this study, we generated a single-contig closed genome assembly with genome-wide DNA methylation profiles for S. parasuis strain A1, isolated from a diseased pig in Xinjiang, China, and complemented in silico genomic predictions with isolate-level experimental validation of antimicrobial resistance (AMR) genotypes, virulence genotypes, and phenotypic susceptibility for this reference strain. Using this high-quality genome as a reference anchor, we performed comparative genomic analyses across 195 streptococcal genomes, comprising 15 S. parasuis and 180 S. suis strains, to distinguish genome-level co-occurrence of resistance and virulence determinants from their physical colocalization on the same mobile genetic element (MGE).Species boundaries remained clearly delineated at the genomic level, with a median interspecies average nucleotide identity (ANI) of approximately 86.0%, compared with intraspecies ANI medians of 97.5% for S. parasuis and 96.2% for S. suis. Pangenome analysis identified 12,693 gene clusters, of which 1086 were core clusters, and functional annotation revealed significant differences in accessory gene repertoires between the two species. Within this stable genomic framework, S. parasuis genomes carried a higher AMR gene burden; strain A1 harbored 10 AMR genes, multiple virulence-associated genes, three genomic islands, and eight prophage regions. For strain A1, PCR validation confirmed six AMR genes and six virulence genes, and disk diffusion testing demonstrated a multidrug-resistant phenotype consistent with the genotypic profile.Among 235 predicted mobile elements, 19 harbored AMR genes and seven carried Virulence Factor Database (VFDB) homologs, but none carried both categories simultaneously. This finding reflects a lack of detectable same-MGE colocalization under the applied annotation and assembly framework; it should not be interpreted as evidence of biological physical decoupling. Under a random-placement model, the expected number of co-carrying regions was only 0.57, and the probability of observing zero co-carrying regions was P = 0.55. This negative result should be interpreted with caution, given the limited number of cargo-bearing regions and the predominantly draft status of most genomes. Furthermore, the A1 genome contained multiple restriction-modification systems, showed depletion of several methylation motif families in mobile regions, and had limited CRISPR spacer matching evidence, suggesting prior exposure to the relevant sequence space. None of the genomes met our predefined criteria for whole-genome convergence.Collectively, our results support a model in which S. parasuis accumulates AMR-related genes in a modular fashion via mobile elements within stable species boundaries, with no detectable same-MGE colocalization of AMR and virulence determinants under our analytical pipeline. These findings imply that AMR surveillance strategies for this species should prioritize tracking mobile genetic elements rather than inferring wholesale genomic convergence toward S. suis.
(Copyright © 2026 Elsevier Ltd. All rights reserved.)
Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. All authors have contributed to the manuscript and approved the final version for submission.
Contributed Indexing: Keywords: Antimicrobial resistance; Comparative genomics; Mobile genetic elements; Species boundary; Streptococcus parasuis; Streptococcus suis
Substance Nomenclature: 0 (Virulence Factors)
0 (Anti-Bacterial Agents)
Entry Date(s): Date Created: 20260828 Date Completed: 20260903 Latest Revision: 20260903
Update Code: 20260904
DOI: 10.1016/j.cimid.2026.102519
PMID: 42664623
Βάση Δεδομένων: MEDLINE
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  Data: Comparative genomic analysis of Streptococcus parasuis and Streptococcus suis reveals mobile element-associated enrichment of antimicrobial resistance and lack of detectable same-MGE colocalization with virulence-associated genes within stable species boundaries.
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  Data: <searchLink fieldCode="AU" term="%22Zhen+Z%22">Zhen Z</searchLink>; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China.<br /><searchLink fieldCode="AU" term="%22Baihe+M%22">Baihe M</searchLink>; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China.<br /><searchLink fieldCode="AU" term="%22Meiliang+G%22">Meiliang G</searchLink>; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China.<br /><searchLink fieldCode="AU" term="%22Yuxuan+W%22">Yuxuan W</searchLink>; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China.<br /><searchLink fieldCode="AU" term="%22Lianrui+L%22">Lianrui L</searchLink>; College of Animal Science and Technology, Tarim University, Alar, Xinjiang, 843300, China; Tarim Animal Husbandry Science and Technology Key Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China; Tarim Animal Disease Diagnosis and Prevention Engineering Laboratory of Xinjiang Production and Construction Corps, Alar, Xinjiang, 843300, China. Electronic address: 15136351829@163.com.
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  Data: Streptococcus suis is a major porcine pathogen and a zoonotic agent that causes meningitis and septicemia in humans. Streptococcus parasuis, a recently recognized close relative, remains poorly characterized with regard to its clinical significance and genomic features. In this study, we generated a single-contig closed genome assembly with genome-wide DNA methylation profiles for S. parasuis strain A1, isolated from a diseased pig in Xinjiang, China, and complemented in silico genomic predictions with isolate-level experimental validation of antimicrobial resistance (AMR) genotypes, virulence genotypes, and phenotypic susceptibility for this reference strain. Using this high-quality genome as a reference anchor, we performed comparative genomic analyses across 195 streptococcal genomes, comprising 15 S. parasuis and 180 S. suis strains, to distinguish genome-level co-occurrence of resistance and virulence determinants from their physical colocalization on the same mobile genetic element (MGE).Species boundaries remained clearly delineated at the genomic level, with a median interspecies average nucleotide identity (ANI) of approximately 86.0%, compared with intraspecies ANI medians of 97.5% for S. parasuis and 96.2% for S. suis. Pangenome analysis identified 12,693 gene clusters, of which 1086 were core clusters, and functional annotation revealed significant differences in accessory gene repertoires between the two species. Within this stable genomic framework, S. parasuis genomes carried a higher AMR gene burden; strain A1 harbored 10 AMR genes, multiple virulence-associated genes, three genomic islands, and eight prophage regions. For strain A1, PCR validation confirmed six AMR genes and six virulence genes, and disk diffusion testing demonstrated a multidrug-resistant phenotype consistent with the genotypic profile.Among 235 predicted mobile elements, 19 harbored AMR genes and seven carried Virulence Factor Database (VFDB) homologs, but none carried both categories simultaneously. This finding reflects a lack of detectable same-MGE colocalization under the applied annotation and assembly framework; it should not be interpreted as evidence of biological physical decoupling. Under a random-placement model, the expected number of co-carrying regions was only 0.57, and the probability of observing zero co-carrying regions was P = 0.55. This negative result should be interpreted with caution, given the limited number of cargo-bearing regions and the predominantly draft status of most genomes. Furthermore, the A1 genome contained multiple restriction-modification systems, showed depletion of several methylation motif families in mobile regions, and had limited CRISPR spacer matching evidence, suggesting prior exposure to the relevant sequence space. None of the genomes met our predefined criteria for whole-genome convergence.Collectively, our results support a model in which S. parasuis accumulates AMR-related genes in a modular fashion via mobile elements within stable species boundaries, with no detectable same-MGE colocalization of AMR and virulence determinants under our analytical pipeline. These findings imply that AMR surveillance strategies for this species should prioritize tracking mobile genetic elements rather than inferring wholesale genomic convergence toward S. suis.<br /> (Copyright © 2026 Elsevier Ltd. All rights reserved.)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. All authors have contributed to the manuscript and approved the final version for submission.
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  Data: <i>Keywords: </i>Antimicrobial resistance; Comparative genomics; Mobile genetic elements; Species boundary; Streptococcus parasuis; Streptococcus suis
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        Value: 10.1016/j.cimid.2026.102519
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        Text: English
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        StartPage: 102519
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      – SubjectFull: Virulence genetics
        Type: general
      – SubjectFull: Virulence Factors genetics
        Type: general
      – SubjectFull: Anti-Bacterial Agents pharmacology
        Type: general
      – SubjectFull: Swine Diseases microbiology
        Type: general
      – SubjectFull: Animals
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      – SubjectFull: Swine
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      – SubjectFull: Microbial Sensitivity Tests
        Type: general
      – SubjectFull: Streptococcus suis genetics
        Type: general
      – SubjectFull: Streptococcus suis drug effects
        Type: general
      – SubjectFull: Streptococcus suis pathogenicity
        Type: general
      – SubjectFull: Interspersed Repetitive Sequences genetics
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      – SubjectFull: Drug Resistance, Bacterial genetics
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      – SubjectFull: Genome, Bacterial
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    Titles:
      – TitleFull: Comparative genomic analysis of Streptococcus parasuis and Streptococcus suis reveals mobile element-associated enrichment of antimicrobial resistance and lack of detectable same-MGE colocalization with virulence-associated genes within stable species boundaries.
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              Text: 2026 Sep
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