Genomics accurately predicts antimicrobial resistance in Staphylococcus pseudintermedius collected as part of Vet-LIRN resistance monitoring

Tyson, Gregory H.; Cerić, Olgica; Guag, Jake; Nemser, Sarah M.; Borenstein, Stacey; Slavić, Ðurđa; Lippert, Sarah; McDowell, Rebecca; Krishnamurthy, Aparna; Korosec, Shannon; Friday, Cheryl; Pople, Neil; Saab, Matthew E.; Fairbrother, Julie-Hélène; Janelle, Isabelle; McMillan, Deanna; Bommineni, Yugendar R.; Simon, David; Mohan, Shipra; Sánchez, Susan; Phillips, Ashley; Bartlett, Paula J.; Naikare, Hemant; Watson, Cynthia K.; Şahin, Orhan; Stinman, Chloe; Wang, Leyi; Maddox, Carol W.; DeShambo, Vanessa; Hendrix, Kenitra; Lubelski, Debra; Burklund, Amy; Lubbers, Brian V.; Reed, Debbie; Jenkins, Tracie M.; Erol, Erdal; Patel, Mukeshbhai; Locke, Stephan; Fortner, Jordan; Peak, Laura; Balasuriya, Udeni B. R.; Mani, Rinosh; Kettler, Niesa; Olsen, Karen Ege; Zhang, Shuping; Shen, Zhenyu; Landinez, Martha Pulido; Thornton, Jay Kay; Thachil, Anil J.; Byrd, Melissa; Jacob, Megan E.; Krogh, Darlene; Webb, Brett T.; Schaan, Lynn; Patil, Amar; Dasgupta, Sarmila; Mann, Shannon; Goodman, Laura B.; Franklin‐Guild, Rebecca J.; Anderson, Renee; Mitchell, Patrick K.; Cronk, Brittany D.; Aprea, Missy; Cui, Jing; Jurkovic, Dominika A.; Prarat, Melanie; Zhang, Yan; Shiplett, Katherine; Campos, Dubra Diaz; Rubio, J.; Ramanchandran, Akhilesh; Talent, Scott; Tewari, Deepanker; Thirumalapura, Nagaraja; Kelly, Douglas G.; Barnhart, Denise; Hall, Lacey; Rankin, Shelley C.; Dietrich, Jaclyn; Cole, Stephen D.; Scaria, Joy; Antony, Linto; Lawhon, Sara D.; Wu, Jing; McCoy, Christine; Dietz, K; Wolking, Rebecca; Alexander, Trevor L.; Burbick, Claire R.; Reimschuessel, Renate

doi:10.1016/j.vetmic.2021.109006

Cited by 16 publications

(25 citation statements)

References 35 publications

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“…This confirmed the high diversity with small lineages, indicating that there is no geographical cluster of Dutch isolates, as they were dispersed over the tree. It also indicated that the lineage associated with CC241 was still overrepresented in human isolates [13,14] (Figure S3). This high diversity in MSSP is in contrast with the observed clonal dissemination of MRSP [13].…”

Section: Discussionmentioning

confidence: 97%

“…The first one was in Europe where 8% of MSSP isolates were MDR and none had genes associated with pRE25-like (erm(B), cat (pC221) , aph(3 )-III, ant6-Ia, sat4) [13]. The second in the USA showed 22.1% MDR among isolates containing erm(B), cat (pC221) , aph(3 )-III, ant6-Ia, sat4, and 11 isolates carried the pRE25-like element [14]. Alignment with this element showed high homology with the pRE25-like elements identified in CC241 isolates in this study, and 4/11 isolates belonged to CC241 and the others belonged to various sequence types.…”

Section: Discussionmentioning

confidence: 99%

“…The genetic relatedness of canine and human MSSP isolates is visualized in a phylogenetic SNP tree of the core genome (size of 2,170,170 bp) in comparison with included publicly available genomes [12][13][14] (Figure 1). This placed our results in a wide epidemiological context and shows that the isolates of this study are dispersed among the high genomic diversity of MSSP isolates.…”

Section: S Pseudintermedius Phylogenymentioning

confidence: 99%

“…In S. pseudintermedius it has been shown that antimicrobial resistance genotypes can accurately predict phenotypical antimicrobial resistances [14,17,18]. Multidrug resistance (MDR) (i.e., carriage of resistance genes to 3 or more classes of antimicrobials) was identified in 13/32 (41%) human isolates and 14/25 (56%) canine isolates (Supplementary Table S1, Figure 1 and Table 1).…”

Section: Antimicrobial Resistance Genesmentioning

confidence: 99%

“…Phylogenetic tree based on the core genome SNPs of MSSP isolates. Publicly available MSSP genomes were compared with the MSSP isolates from this study, that have been marked red for human isolates and blue for dog isolates[12][13][14].…”

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confidence: 99%

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Absence of Host-Specific Genes in Canine and Human Staphylococcus pseudintermedius as Inferred from Comparative Genomics

et al. 2021

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Staphylococcus pseudintermedius is an important pathogen in dogs that occasionally causes infections in humans as an opportunistic pathogen of elderly and immunocompromised people. This study compared the genomic relatedness and antimicrobial resistance genes using genome-wide association study (GWAS) to examine host association of canine and human S. pseudintermedius isolates. Canine (n = 25) and human (n = 32) methicillin-susceptible S. pseudintermedius (MSSP) isolates showed a high level of genetic diversity with an overrepresentation of clonal complex CC241 in human isolates. This clonal complex was associated with carriage of a plasmid containing a bacteriocin with cytotoxic properties, a CRISPR-cas domain and a pRE25-like mobile element containing five antimicrobial resistance genes. Multi-drug resistance (MDR) was predicted in 13 (41%) of human isolates and 14 (56%) of canine isolates. CC241 represented 54% of predicted MDR isolates from humans and 21% of predicted MDR canine isolates. While it had previously been suggested that certain host-specific genes were present the current GWAS analysis did not identify any genes that were significantly associated with human or canine isolates. In conclusion, this is the first genomic study showing that MSSP is genetically diverse in both hosts and that multidrug resistance is important in dog and human-associated S. pseudintermedius isolates.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: S Pseudintermedius Phylogenymentioning

confidence: 99%

Section: Antimicrobial Resistance Genesmentioning

confidence: 99%

mentioning

confidence: 99%

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Absence of Host-Specific Genes in Canine and Human Staphylococcus pseudintermedius as Inferred from Comparative Genomics

et al. 2021

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Molecular characterization of high-level mupirocin resistance in methicillin-resistant staphylococci isolated from companion animals

Kizerwetter-Świda

Chrobak-Chmiel

Kwiecień

et al. 2021

Veterinary Microbiology

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Diagnostic and commensal Staphylococcus pseudintermedius genomes reveal niche adaptation through parallel selection of defense mechanisms

Sawhney,

Vargas,

Wallace

et al. 2023

Nat Commun

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Staphylococcus pseudintermedius is historically understood as a prevalent commensal and pathogen of dogs, though modern clinical diagnostics reveal an expanded host-range that includes humans. It remains unclear whether differentiation across S. pseudintermedius populations is driven primarily by niche-type or host-species. We sequenced 501 diagnostic and commensal isolates from a hospital, veterinary diagnostic laboratory, and within households in the American Midwest, and performed a comparative genomics investigation contrasting human diagnostic, animal diagnostic, human colonizing, pet colonizing, and household-surface S. pseudintermedius isolates. Though indistinguishable by core and accessory gene architecture, diagnostic isolates harbor more encoded and phenotypic resistance, whereas colonizing and surface isolates harbor similar CRISPR defense systems likely reflective of common household phage exposures. Furthermore, household isolates that persist through anti-staphylococcal decolonization report elevated rates of base-changing mutations in – and parallel evolution of – defense genes, as well as reductions in oxacillin and trimethoprim-sulfamethoxazole susceptibility. Together we report parallel niche-specific bolstering of S. pseudintermedius defense mechanisms through gene acquisition or mutation.

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Genomics accurately predicts antimicrobial resistance in Staphylococcus pseudintermedius collected as part of Vet-LIRN resistance monitoring

Cited by 16 publications

References 35 publications

Absence of Host-Specific Genes in Canine and Human Staphylococcus pseudintermedius as Inferred from Comparative Genomics

Absence of Host-Specific Genes in Canine and Human Staphylococcus pseudintermedius as Inferred from Comparative Genomics

Molecular characterization of high-level mupirocin resistance in methicillin-resistant staphylococci isolated from companion animals

Diagnostic and commensal Staphylococcus pseudintermedius genomes reveal niche adaptation through parallel selection of defense mechanisms

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