Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019
ABSTRACT Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) clonal complex 398 (CC398) isolates (n = 178) collected in the national resistance monitoring program GERM-Vet from diseased swine in Germany from 2007 to 2019 were investigated for their genomic diversity with a foc...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-06-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00770-23 |
| _version_ | 1797803374329987072 |
|---|---|
| author | Henrike Krüger-Haker Xing Ji Dennis Hanke Stefan Fiedler Andrea T. Feßler Nansong Jiang Heike Kaspar Yang Wang Congming Wu Stefan Schwarz |
| author_facet | Henrike Krüger-Haker Xing Ji Dennis Hanke Stefan Fiedler Andrea T. Feßler Nansong Jiang Heike Kaspar Yang Wang Congming Wu Stefan Schwarz |
| author_sort | Henrike Krüger-Haker |
| collection | DOAJ |
| description | ABSTRACT Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) clonal complex 398 (CC398) isolates (n = 178) collected in the national resistance monitoring program GERM-Vet from diseased swine in Germany from 2007 to 2019 were investigated for their genomic diversity with a focus on virulence and antimicrobial resistance (AMR) traits. Whole-genome sequencing was followed by molecular typing and sequence analysis. A minimum spanning tree based on core-genome multilocus sequence typing was constructed, and antimicrobial susceptibility testing was performed. Most isolates were assigned to nine clusters. They displayed close phylogenetic relationships but a wide molecular variety, including 13 spa types and 19 known and four novel dru types. Several toxin-encoding genes, including eta, seb, sek, sep, and seq, were detected. The isolates harbored a wide range of AMR properties mirroring the proportions of the classes of antimicrobial agents applied in veterinary medicine in Germany. Multiple novel or rare AMR genes were identified, including the phenicol-lincosamide-oxazolidinone-pleuromutilin-streptogramin A resistance gene cfr, the lincosamide-pleuromutilin-streptogramin A resistance gene vga(C), and the novel macrolide-lincosamide-streptogramin B resistance gene erm(54). Many AMR genes were part of small transposons or plasmids. Clonal and geographical correlations of molecular characteristics and resistance and virulence genes were more frequently observed than temporal relations. In conclusion, this study provides insight into population dynamics of the main epidemic porcine LA-MRSA lineage in Germany over a 13-year-period. The observed comprehensive AMR and virulence properties, most likely resulting from the exchange of genetic material between bacteria, highlighted the importance of LA-MRSA surveillance to prevent further dissemination among swine husbandry facilities and entry into the human community. IMPORTANCE The LA-MRSA-CC398 lineage is known for its low host specificity and frequent multiresistance to antimicrobial agents. Colonized swine and their related surroundings represent a considerable risk of LA-MRSA-CC398 colonization or infection for occupationally exposed people through which such isolates might be further disseminated within the human community. This study provides insight into the diversity of the porcine LA-MRSA-CC398 lineage in Germany. Clonal and geographical correlations of molecular characteristics and resistance and virulence traits were detected and may be associated with the spread of specific isolates through livestock trade, human occupational exposure, or dust emission. The demonstrated genetic variability underlines the lineage’s ability to horizontally acquire foreign genetic material. Thus, LA-MRSA-CC398 isolates have the potential to become even more dangerous for various host species, including humans, due to increased virulence and/or limited therapeutic options for infection control. Full-scale LA-MRSA monitoring at the farm, community, and hospital level is therefore essential. |
| first_indexed | 2024-03-13T05:19:53Z |
| format | Article |
| id | doaj.art-1789359928c745dfa28ecb3ed332d514 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:19:53Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-1789359928c745dfa28ecb3ed332d5142023-06-15T13:18:33ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.00770-23Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019Henrike Krüger-Haker0Xing Ji1Dennis Hanke2Stefan Fiedler3Andrea T. Feßler4Nansong Jiang5Heike Kaspar6Yang Wang7Congming Wu8Stefan Schwarz9Institute of Microbiology and Epizootics, Centre for Infection Medicine, School of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyJiangsu Key Laboratory for Food Quality and Safety, State Key Laboratory, Cultivation Base of Ministry of Science and Technology, Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaInstitute of Microbiology and Epizootics, Centre for Infection Medicine, School of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyFederal Office of Consumer Protection and Food Safety (BVL), Berlin, GermanyInstitute of Microbiology and Epizootics, Centre for Infection Medicine, School of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyKey Laboratory of Animal Antimicrobial Resistance Surveillance, MARA, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaFederal Office of Consumer Protection and Food Safety (BVL), Berlin, GermanyKey Laboratory of Animal Antimicrobial Resistance Surveillance, MARA, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaKey Laboratory of Animal Antimicrobial Resistance Surveillance, MARA, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaInstitute of Microbiology and Epizootics, Centre for Infection Medicine, School of Veterinary Medicine, Freie Universität Berlin, Berlin, GermanyABSTRACT Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) clonal complex 398 (CC398) isolates (n = 178) collected in the national resistance monitoring program GERM-Vet from diseased swine in Germany from 2007 to 2019 were investigated for their genomic diversity with a focus on virulence and antimicrobial resistance (AMR) traits. Whole-genome sequencing was followed by molecular typing and sequence analysis. A minimum spanning tree based on core-genome multilocus sequence typing was constructed, and antimicrobial susceptibility testing was performed. Most isolates were assigned to nine clusters. They displayed close phylogenetic relationships but a wide molecular variety, including 13 spa types and 19 known and four novel dru types. Several toxin-encoding genes, including eta, seb, sek, sep, and seq, were detected. The isolates harbored a wide range of AMR properties mirroring the proportions of the classes of antimicrobial agents applied in veterinary medicine in Germany. Multiple novel or rare AMR genes were identified, including the phenicol-lincosamide-oxazolidinone-pleuromutilin-streptogramin A resistance gene cfr, the lincosamide-pleuromutilin-streptogramin A resistance gene vga(C), and the novel macrolide-lincosamide-streptogramin B resistance gene erm(54). Many AMR genes were part of small transposons or plasmids. Clonal and geographical correlations of molecular characteristics and resistance and virulence genes were more frequently observed than temporal relations. In conclusion, this study provides insight into population dynamics of the main epidemic porcine LA-MRSA lineage in Germany over a 13-year-period. The observed comprehensive AMR and virulence properties, most likely resulting from the exchange of genetic material between bacteria, highlighted the importance of LA-MRSA surveillance to prevent further dissemination among swine husbandry facilities and entry into the human community. IMPORTANCE The LA-MRSA-CC398 lineage is known for its low host specificity and frequent multiresistance to antimicrobial agents. Colonized swine and their related surroundings represent a considerable risk of LA-MRSA-CC398 colonization or infection for occupationally exposed people through which such isolates might be further disseminated within the human community. This study provides insight into the diversity of the porcine LA-MRSA-CC398 lineage in Germany. Clonal and geographical correlations of molecular characteristics and resistance and virulence traits were detected and may be associated with the spread of specific isolates through livestock trade, human occupational exposure, or dust emission. The demonstrated genetic variability underlines the lineage’s ability to horizontally acquire foreign genetic material. Thus, LA-MRSA-CC398 isolates have the potential to become even more dangerous for various host species, including humans, due to increased virulence and/or limited therapeutic options for infection control. Full-scale LA-MRSA monitoring at the farm, community, and hospital level is therefore essential.https://journals.asm.org/doi/10.1128/spectrum.00770-23LA-MRSAevolutionantimicrobial resistance monitoringwhole-genome sequencingcgMLSTantimicrobial susceptibility testing |
| spellingShingle | Henrike Krüger-Haker Xing Ji Dennis Hanke Stefan Fiedler Andrea T. Feßler Nansong Jiang Heike Kaspar Yang Wang Congming Wu Stefan Schwarz Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019 Microbiology Spectrum LA-MRSA evolution antimicrobial resistance monitoring whole-genome sequencing cgMLST antimicrobial susceptibility testing |
| title | Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019 |
| title_full | Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019 |
| title_fullStr | Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019 |
| title_full_unstemmed | Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019 |
| title_short | Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019 |
| title_sort | genomic diversity of methicillin resistant staphylococcus aureus cc398 isolates collected from diseased swine in the german national resistance monitoring program germ vet from 2007 to 2019 |
| topic | LA-MRSA evolution antimicrobial resistance monitoring whole-genome sequencing cgMLST antimicrobial susceptibility testing |
| url | https://journals.asm.org/doi/10.1128/spectrum.00770-23 |
| work_keys_str_mv | AT henrikekrugerhaker genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT xingji genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT dennishanke genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT stefanfiedler genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT andreatfeßler genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT nansongjiang genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT heikekaspar genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT yangwang genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT congmingwu genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 AT stefanschwarz genomicdiversityofmethicillinresistantstaphylococcusaureuscc398isolatescollectedfromdiseasedswineinthegermannationalresistancemonitoringprogramgermvetfrom2007to2019 |