A Survey of Chinese Pig Farms and Human Healthcare Isolates Reveals Separate Human and Animal Methicillin‐Resistant <i>Staphylococcus aureus</i> Populations

Zou, Geng; Matuszewska, Marta; Jia, Ming; Zhou, Jianwei; Ba, Xiaoliang; Duan, Juan; Zhang, Caishi; Zhao, Jian; Tao, Meifeng; Jia, Fan; Zhang, Xiangming; Jin, Wenping; Cui, Tengfei; Zeng, Xianyu; Jia, Min; Qian, X.; Huang, Chao; Zhuo, Wenxiao; Yao, Zhiming; Zhang, Lijun; Li, Shaowen; Li, Lü; Huang, Qi; Wu, Bin; Chen, Huanchun; Tucker, Alexander W.; Grant, A.; Holmes, Mark A.; Zhou, Rui

doi:10.1002/advs.202103388

Cited by 15 publications

(14 citation statements)

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“…Previous studies suggest that LA-MRSA CC398 emerged from human-associated methicillin-sensitive S. aureus (MSSA) ( Price et al, 2012 ). However, the presence of SCC mec elements in recently sampled human-associated CC398 isolates that fall basal to the livestock-associated clade, including clinical isolates from China ( He et al, 2018 ; Zou et al, 2022 ), Denmark ( Moller et al, 2019 ), and New Zealand ( Gonçalves da Silva et al, 2017 ), makes the association between methicillin resistance and livestock association less clear ( Figure 1a ).…”

Section: Resultsmentioning

confidence: 99%

Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA

Matuszewska

Murray

et al. 2022

eLife

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Mobile genetic elements (MGEs) are agents of horizontal gene transfer in bacteria, but can also be vertically inherited by daughter cells. Establishing the dynamics that led to contemporary patterns of MGEs in bacterial genomes is central to predicting the emergence and evolution of novel and resistant pathogens. Methicillin-resistant Staphylococcus aureus (MRSA) clonal-complex (CC) 398 is the dominant MRSA in European livestock and a growing cause of human infections. Previous studies have identified three categories of MGEs whose presence or absence distinguishes livestock-associated CC398 from a closely related and less antibiotic-resistant human-associated population. Here, we fully characterise the evolutionary dynamics of these MGEs using a collection of 1180 CC398 genomes, sampled from livestock and humans, over 27 years. We find that the emergence of livestock-associated CC398 coincided with the acquisition of a Tn916 transposon carrying a tetracycline resistance gene, which has been stably inherited for 57 years. This was followed by the acquisition of a type V SCCmec that carries methicillin, tetracycline, and heavy metal resistance genes, which has been maintained for 35 years, with occasional truncations and replacements with type IV SCCmec. In contrast, a class of prophages that carry a human immune evasion gene cluster and that are largely absent from livestock-associated CC398 have been repeatedly gained and lost in both human- and livestock-associated CC398. These contrasting dynamics mean that when livestock-associated MRSA is transmitted to humans, adaptation to the human host outpaces loss of antibiotic resistance. In addition, the stable inheritance of resistance-associated MGEs suggests that the impact of ongoing reductions in antibiotic and zinc oxide use in European farms on livestock-associated MRSA will be slow to be realised.

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Section: Resultsmentioning

confidence: 99%

Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA

Matuszewska

Murray

et al. 2022

eLife

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“…Previous studies suggest that LA-MRSA CC398 emerged from human-associated MSSA (Price et al 2012). However, the presence of SCC mec elements in recently sampled human-associated CC398 isolates that fall basal to the livestock-associated clade, including clinical isolates from China (He et al 2018; Zou et al 2022), Denmark (Møller et al 2019), and New Zealand (Silva et al 2017), makes the association between methicillin-resistance and livestock-association less clear (Figure 1a).…”

Section: Resultsmentioning

confidence: 99%

Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA

Matuszewska

Murray

et al. 2021

Preprint

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Mobile genetic elements (MGEs) often carry genes that benefit their bacterial hosts. In methicillin-resistant Staphylococcus aureus (MRSA), MGEs have been associated with antibiotic resistance, virulence, and host adaptation. Clonal-complex (CC) 398 is the dominant MRSA in European livestock, and a growing cause of human infections. To understand the risk posed by livestock-associated MRSA to human health, we have used a collection of 1,180 CC398 genomes, sampled from several livestock species and humans, with a broad geographic distribution and spanning 27 years, to reconstruct the dynamics of the MGEs. We find that the emergence of livestock-associated CC398 coincided with the acquisition of a Tn916 transposon carrying a tetracycline resistance gene, which has been stably vertically inherited for 57 years. This was followed by the acquisition of a large SCCmec type V element that carries methicillin, tetracycline and heavy metal resistance genes. This has been maintained within livestock-associated CC398 for at least 35 years, with occasional truncations and replacements with other, smaller type IV SCCmec elements. In contrast, a class of prophages that carry a human immune-evasion gene cluster, that are largely absent from livestock-associated CC398, have been repeatedly gained and lost across both human- and livestock-associated CC398. The variable dynamics of these three MGEs means that when livestock-associated MRSA infects humans, re-adaptation to the human host outpaces the loss of antibiotic resistance. Moreover, the stability of both Tn916 and SCCmec suggests that they may persist despite ongoing reductions in antibiotic and zinc oxide use in farming.

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“…More important CA-MRSA clones according to [ 2 , 23 , 217 , 218 , 219 , 220 , 221 , 222 , 223 , 224 , 225 , 226 , 227 , 228 , 229 , 230 , 231 , 232 ] are shown in Table 4 , most important HA-MRSA clones according to [ 23 , 85 , 125 , 220 , 224 , 233 , 234 , 235 , 236 ] are shown in Table 5 , and most important LA-MRSA clones according to [ 23 , 125 , 237 , 238 , 239 , 240 , 241 , 242 ] are shown in Table 6 .…”

Section: Molecular Epidemiology Of Mrsamentioning

confidence: 99%

Molecular Mechanisms of Drug Resistance in Staphylococcus aureus

Młynarczyk-Bonikowska

Kowaléwski

Krolak-Ulinska³

et al. 2022

IJMS

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This paper discusses the mechanisms of S. aureus drug resistance including: (1) introduction. (2) resistance to beta-lactam antibiotics, with particular emphasis on the mec genes found in the Staphylococcaceae family, the structure and occurrence of SCCmec cassettes, as well as differences in the presence of some virulence genes and its expression in major epidemiological types and clones of HA-MRSA, CA-MRSA, and LA-MRSA strains. Other mechanisms of resistance to beta-lactam antibiotics will also be discussed, such as mutations in the gdpP gene, BORSA or MODSA phenotypes, as well as resistance to ceftobiprole and ceftaroline. (3) Resistance to glycopeptides (VRSA, VISA, hVISA strains, vancomycin tolerance). (4) Resistance to oxazolidinones (mutational and enzymatic resistance to linezolid). (5) Resistance to MLS-B (macrolides, lincosamides, ketolides, and streptogramin B). (6) Aminoglycosides and spectinomicin, including resistance genes, their regulation and localization (plasmids, transposons, class I integrons, SCCmec), and types and spectrum of enzymes that inactivate aminoglycosides. (7). Fluoroquinolones (8) Tetracyclines, including the mechanisms of active protection of the drug target site and active efflux of the drug from the bacterial cell. (9) Mupirocin. (10) Fusidic acid. (11) Daptomycin. (12) Resistance to other antibiotics and chemioterapeutics (e.g., streptogramins A, quinupristin/dalfopristin, chloramphenicol, rifampicin, fosfomycin, trimethoprim) (13) Molecular epidemiology of MRSA.

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A Survey of Chinese Pig Farms and Human Healthcare Isolates Reveals Separate Human and Animal Methicillin‐Resistant Staphylococcus aureus Populations

Cited by 15 publications

References 58 publications

Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA

Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA

Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA

Molecular Mechanisms of Drug Resistance in Staphylococcus aureus

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