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Background A livestock-associated clonal lineage (ST398) of methicillin-resistant Staphylococcus aureus (MRSA) has been identified causing colonization or infection in farm workers. The aim of the study was to analyze the prevalence of MRSA-ST398 colonization in pigs and in pig farmers in an area with a high pig population (Osona, Barcelona province, Catalonia, Spain). Methods We performed a cross-sectional prevalence study in Osona (Catalonia, Spain), from June 2014 to June 2015. All pig farm workers from 83 farms were studied. Twenty of these farms were randomly selected for the study of both pigs and farmers: 9 fattening and 11 farrow-to-finish farms. All workers over the age of 18 who agreed to participate were included. Samples were analyzed to identify MRSA-ST398 and their spa type. Results Eighty-one of the 140 pig farm workers analyzed (57.9% (95% IC: 50.0–66.4%)) were MRSA-positive, all of them ST398. The mean number of years worked on farms was 17.5 ± 12.6 (range:1–50), without significant differences between positive and negative MRSA results ( p  = 0.763). Over 75% of MRSA-ST398 carriers worked on farms with more than 1250 pigs ( p  < 0.001). At least one worker tested positive for MRSA-ST398 on all 20 selected pig farms. Ninety-two (46.0% (95% IC: 39.0–53.0%)) of the nasal swabs from 200 pigs from these 20 farms were MRSA-positive, with 50.5% of sows and 41.4% of fattening pigs ( p  = 0.198) giving MRSA-positive results. All the isolates were tetracycline-resistant, and were identified as MRSA-ST398. The spa type identified most frequently was t011 (62%). Similar spa types and phenotypes of antibiotic resistance were identified in pigs and farmers of 19/20 tested farms. Conclusions The prevalence of MRSA-ST398 among pig farm workers and pigs on farms in the studied region is very high, and the size of the farm seems to correlate with the frequency of colonization of farmers. The similar spa -types and phenotypes of resistance detected in pigs and workers in most of the farms studied suggest animal-to-human transmission.

( ) is a notorious pathogen that cause metastatic or complicated infections. Hypervirulent ST398 clonotype strains, remarkably increased in recent years, dominated Community-associated (CA-SA) infections in the past decade in China. Small RNAs like RNAIII have been demonstrated to play important roles in regulating the virulence of , however, the regulatory roles played by many of these sRNAs in the ST398 clonotype strains are still unclear. Through transcriptome screening and combined with knockout phenotype analysis, we have identified a highly transcribed sRNA, RSaX28, in the ST398 clonotype strains. Sequence analysis revealed that RSaX28 is highly conserved in the most epidemic clonotypes of , but its high transcription level is particularly prominent in the ST398 clonotype strains. Characterization of RSaX28 through RACE and Northern blot revealed its length to be 533nt. RSaX28 is capable of promoting the hemolytic ability, reducing biofilm formation capacity, and enhancing virulence of in the murine infection model. Through IntaRNA prediction and EMSA validation, we found that RSaX28 can specifically interact with RNAIII, promoting its stability and positively regulating the translation of downstream alpha-toxin while inhibiting the translation of Sbi, thereby regulating the virulence and biofilm formation capacity of the ST398 clonotype strains. RSaX28 is an important virulence regulatory factor in the ST398 clonotype and represents a potential important target for future treatment and immune intervention against infections.

Livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 (LA-MRSA CC398) is resistant to nearly all β-lactams and several non-β-lactam antimicrobials. Over the last decade, it has become widespread in pig farms across Europe and is now an important cause of human infections in countries with previously low levels of MRSA, such as the Netherlands and Denmark. The hitherto uncontrolled spread of LA-MRSA CC398 underscores an urgent need to understand its epidemiology in order to develop evidence-based interventions. This study demonstrates that pig movements between farms in combination with increased bacterial resistance to specific antibiotics and heavy metals were important drivers of the rapid spread of LA-MRSA CC398 in the Danish pig production system. These findings should be taken into consideration when researchers and policy makers evaluate and decide on actions and policies to limit the spread of LA-MRSA CC398 and other pathogens in food animals. The spread of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 (LA-MRSA CC398) within the Danish pig production system has been linked to an increased number of human infections. Yet, the population structure and transmission dynamics of this important pathogen remain poorly understood. In this study, whole-genome sequences from 371 LA-MRSA CC398 isolates collected between 2004 and 2015 were subjected to bioinformatic analyses. The isolates originated from Danish pig farms ( n = 209) and people having livestock contact ( n = 79). In addition, whole-genome sequence data from 82 isolates representing an international reference collection and 83 isolates from Danish patients were included in the analysis. The results demonstrated that the increasing prevalence of LA-MRSA CC398 in Danish pigs and patients was caused by clonal expansion of three dominant lineages. The results also showed that these lineages were enriched for the tetracycline resistance gene tet (K) and other determinants conferring resistance to some of the most frequently used antimicrobials in Danish pigs. The association between pig movements and the spread of LA-MRSA CC398 was assessed in a Poisson regression analysis of 17,009 pig movements into 273 farms with known LA-MRSA CC398 status. The results demonstrated that animal movements have played a critical role in the dissemination of LA-MRSA CC398 within the Danish pig production system, although other transmission routes may also have contributed. Consistent with this scenario, the genetic relatedness of isolates from different farms was positively correlated with the number of animal movements between the farms. IMPORTANCE Livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 (LA-MRSA CC398) is resistant to nearly all β-lactams and several non-β-lactam antimicrobials. Over the last decade, it has become widespread in pig farms across Europe and is now an important cause of human infections in countries with previously low levels of MRSA, such as the Netherlands and Denmark. The hitherto uncontrolled spread of LA-MRSA CC398 underscores an urgent need to understand its epidemiology in order to develop evidence-based interventions. This study demonstrates that pig movements between farms in combination with increased bacterial resistance to specific antibiotics and heavy metals were important drivers of the rapid spread of LA-MRSA CC398 in the Danish pig production system. These findings should be taken into consideration when researchers and policy makers evaluate and decide on actions and policies to limit the spread of LA-MRSA CC398 and other pathogens in food animals.

Staphylococcus aureus is one of the most important pathogens in humans as well as in livestock. Particularly, bovine mastitis caused by S. aureus is a serious issue in dairy farms due to disease recurrence. Here, cases of S. aureus-mediated intramammary infection occurring in the Miyagi Prefecture in Japan were monitored from May 2015 to August 2019; a total of 59 strains (49 from bovine milk and 10 from bulk milk) were obtained from 15 dairy farms and analyzed via sequence-based typing methods and antibiotic susceptibility tests. Two pairs of isolates were determined as recurrence cases from the same cows in distinct farms. The sequence type (ST), spa type, and coa type of each pair were the same: one pair showed ST705, t529, and VIb and the other showed ST352, t267, and VIc. In addition, the possession of toxin genes analyzed of each pair was exactly the same. Furthermore, seven oxacillin-sensitive clonal complex 398 isolates were obtained from a single farm. This is the first confirmed case of a Methicillin-Sensitive SA (MSSA) ST398 strain isolated from mastitis-containing cows in Japan. Our findings suggest that nationwide surveillance of the distribution of ST398 strains in dairy farms is important for managing human and animal health.

Staphylococcus aureus (SA) belonging to the clonal complex 398 (CC398) took a special place within the species due to its spread throughout the world. SA CC398 is broadly separated in two subpopulations: livestock-associated methicillin-resistant SA (MRSA) and human-associated methicillin-susceptible SA (MSSA). Here, we reviewed the global epidemiology of SA CC398 in human clinical infections and focused on MSSA CC398. The last common ancestor of SA CC398 was probably a human-adapted prophage φSa3-positive MSSA CC398 strain, but the multiple transmissions between human and animal made its evolution complex. MSSA and MRSA CC398 had different geographical evolutions. Although MSSA was present in several countries all over the world, it was mainly reported in China and in France with a prevalence about 20%. MSSA CC398 was frequently implicated in severe infections such as bloodstream infections, endocarditis, and bone joint infections whereas MRSA CC398 was mainly reported in skin and soft tissue. The spread of the MSSA CC398 clone is worldwide but with a heterogeneous prevalence. The prophage φSa3 played a crucial role in the adaptation to the human niche and in the virulence of MSSA CC398. However, the biological features that allowed the recent spread of this lineage are still far from being fully understood.

Livestock-associated Staphylococcus aureus ST398 is a highly pathogenic species that causes infections in a wide variety of animals, including humans. The bacteriophage (phage) vB_SauS_S1 was isolated originally using a ST398 strain as its “isolating host”, then the spot tests showed it was able to infect 73.33% (22/30) ST398 isolates. Phage S1 was assigned as a temperate phage based on genome analysis and phenotypic validation. Phylogenetic analysis showed that S1 was closely related to temperate phages tp310-2 and SA137ruMSSAST121PVL. Following infection of ST398 by phage S1, the lysogenic strain showed enhanced biofilm forming ability compared to the wildtype strain, and the invasion rate of MAC-T cells increased by 10.39%. The minimum inhibitory concentration showed that phage S1 did not change the antibiotic sensitivity of the lysogen strain, and the virulence of the lysogen strain did not change significantly in the injection models of Galleria mellonella ( G. mellonella ) and mice. The lysogen demonstrated superinfection immunity and reduced sensitivity to virulent phage infection. Thus, this study contributes to understanding the co-evolutionary relationships between temperate phages and the multi-host zoonotic pathogen S. aureus ST398.

Methicillin-resistant Staphylococcus aureus (MRSA) of sequence types ST398 and ST9 are dominant lineages among livestock in Europe and Asia, respectively. Although both STs were commonly found as colonizers of the skin and the mucosal membranes, MRSA ST398, rather than MRSA ST9, has been reported to cause infections in humans and animals. Herein, we comparatively analyzed the genomic characteristics, fitness and virulence of MRSA ST398 and ST9 isolated from pigs in both China (CHN) and Germany (GER) to explore the factors that lead to differences in their epidemics and pathogenicity. We observed that the CHN-MRSA ST9 and the GER-MRSA ST9 have evolved independently, whereas the CHN-MRSA ST398 and GER-MRSA ST398 had close evolutionary relationships. Resistance to antimicrobial agents commonly used in livestock, the enhanced ability of biofilm formation, and the resistance to desiccation contribute to the success of the dominant clones of CHN-MRSA ST9 and GER-MRSA ST398, and the vwb νSaα gene on the genomic island might in part contribute to their colonization fitness in pigs. All MRSA ST398 strains revealed more diverse genome structures, higher tolerance to acids and high osmotic pressure, and greater competitive fitness in co-culture experiments. Notably, we identified and characterized a novel hysA νSaβ gene, which was located on the genomic island νSaβ of MRSA ST398 but was absent in MRSA ST9. The enhanced pathogenicity of the MRSA ST398 strains due to hysA νSaβ might in part explain why MRSA ST398 strains are more likely to cause infections.

Background Severe infections with highly virulent community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) are a global problem. However, the molecular events defining the evolution of CA-MRSA are still poorly understood. MRSA of sequence type (ST) 398 is known to frequently infect livestock, while ST398 isolates infecting humans are commonly methicillin-susceptible or represent MRSA originating from livestock-associated (LA)-MRSA. Methods We used whole genome sequencing of newly detected CA-MRSA ST398 isolates, in comparison to geographically matched LA-MRSA and methicillin-sensitive ST398, to determine their evolutionary history. Furthermore, we used phenotypic analyses including animal infection models to gain insight into the evolution of virulence in these CA-MRSA isolates. Finally, we determined methicillin resistance and expression of the methicillin resistance-conferring gene mecA and its penicillin-binding protein product, PBP2a, in a large series of CA-MRSA strains of divergent STs. Results We report several cases of severe and fatal infections due to ST398 CA-MRSA. The responsible isolates showed the typical genetic characteristics reported for human-adapted methicillin-sensitive ST398. Whole genome sequencing demonstrated that they evolved from human-adapted, methicillin-susceptible clones on several different occasions. Importantly, the isolates had not undergone consistent genetic alterations or changes in virulence as compared to their methicillin-susceptible predecessors. Finally, we observed dramatically and consistently lower methicillin resistance and expression of the resistance gene mecA , as compared to hospital-associated MRSA strains, in a diverse selection of CA-MRSA strains. Conclusions Our study presents evidence for the development of highly virulent human-adapted ST398 CA-MRSA isolates from methicillin-susceptible predecessors. Notably, our investigation indicates that, in contrast to widespread notions, the development of CA-MRSA is not necessarily associated with the acquisition of specific virulence genes or other virulence-increasing changes. Rather, our findings emphasize the importance of the CA-MRSA-characteristic staphylococcal cassette chromosome mec types, which provide only low-level methicillin resistance, for that process. Our findings are of particular importance for the diagnosis of CA-MRSA, inasmuch as they indicate that the presence of specific virulence genes cannot generally be used for that purpose.

There has been increasing concern that the overuse of antibiotics in livestock farming is contributing to the burden of antimicrobial resistance in people. Farmed animals in Europe and North America, particularly pigs, provide a reservoir for livestock‐associated methicillin‐resistant Staphylococcus aureus (LA‐MRSA ST398 lineage) found in people. This study is designed to investigate the contribution of MRSA from Chinese pig farms to human infection. A collection of 483 MRSA are isolated from 55 farms and 4 hospitals in central China, a high pig farming density area. CC9 MRSA accounts for 97.2% of all farm isolates, but is not present in hospital isolates. ST398 isolates are found on farms and hospitals, but none of them formed part of the “LA‐MRSA ST398 lineage” present in Europe and North America. The hospital ST398 MRSA isolate form a clade that is clearly separate from the farm ST398 isolates. Despite the presence of high levels of MRSA found on Chinese pig farms, the authors find no evidence of them spilling over to the human population. Nevertheless, the ST398 MRSA obtained from hospitals appear to be part of a widely distributed lineage in China. The new animal‐adapted ST398 lineage that has emerged in China is of concern. Zoonotic transmission of methicillin‐resistant Staphylococcus aureus (MRSA) is a significant problem and adds to the burden on antibiotic resistance in human healthcare. However, population‐level genomic studies reveal a separate MRSA population between farmed pigs and people in central China, a high pig farming density area.

Background: Staphylococcus aureus is one of the predominant causes of skin and soft tissue infections (SSTIs), but limited data were available regarding the characterization of S. aureus from SSTIs patients in Jiangsu Province in China. We aimed to investigate the molecular epidemiology of S. aureus among SSTIs patients in two hospitals of Jiangsu Province. Methods: Sixty-two patients with SSTIs from two Chinese hospitals in Jiangsu Province were enrolled in this study, and 62 S. aureus isolates were collected from February 2014 to January 2015. S. aureus isolates were characterized by antimicrobial susceptibility testing, toxin gene detection, and molecular typing with sequence type, Staphylococcus protein A gene type, accessory gene regulator (agr) group, and Staphylococcal cassette chromosome mec t ype. Results: Sixteen (25.8%) methicillin-resistant S. aureus (MRSA) isolates were detected, and there was no isolate found resistant to vancomycin, teicoplanin, sulfamethoxazole-trimethoprim, and linezolid. The sei was the toxin gene most frequently found, and no lukS/F-PV-positive isolates were detected among the SSTIs' patients. Molecular analysis revealed that ST398 (10/62, 16.1%; 2 MRSA and 8 methicillin-susceptible S. aureus) to be the dominant clone, followed by ST5 (8/62, 12.9%) and ST7 (8/62, 12.9%). Conclusions: The livestock ST398 was the most common clone among patients with S. aureus SSTIs in Jiangsu Province, China. Surveillance and further studies on the important livestock ST398 clone in human infections are necessarily requested.