Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans
Abstract Multidrug-resistant (MDR) Salmonella has been a long-standing challenge in public health and food safety. The prevalence of MDR S. Enteritidis, especially isolated from humans, in China is significantly higher than those from the U.S. and other countries. A dataset of 197 S. Enteritidis gen...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-01-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-24150-4 |
| _version_ | 1811175879776141312 |
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| author | Guojie Cao Shaohua Zhao Dai Kuang Chih-Hao Hsu Lanlan Yin Yan Luo Zhao Chen Xuebin Xu Errol Strain Patrick McDermott Marc Allard Eric Brown Jianghong Meng Jie Zheng |
| author_facet | Guojie Cao Shaohua Zhao Dai Kuang Chih-Hao Hsu Lanlan Yin Yan Luo Zhao Chen Xuebin Xu Errol Strain Patrick McDermott Marc Allard Eric Brown Jianghong Meng Jie Zheng |
| author_sort | Guojie Cao |
| collection | DOAJ |
| description | Abstract Multidrug-resistant (MDR) Salmonella has been a long-standing challenge in public health and food safety. The prevalence of MDR S. Enteritidis, especially isolated from humans, in China is significantly higher than those from the U.S. and other countries. A dataset of 197 S. Enteritidis genomes, including 16 sequenced clinical isolates from China and 181 downloaded genomes of human isolates from the U.S., Europe, and Africa, was analyzed for genomic diversity, virulence potential, and antimicrobial resistance (AMR). Phylogenomic analyses identified four major well-supported clades (I–IV). While AMR genotype in the majority of isolates in clades I and IV displayed as pan-susceptible, 81.8% (9/11) and 22.4% (13/58) of isolates in clades III and II were MDR, respectively. It is noted that 77% (10/13) of MDR isolates in clade II were from China. The most common antimicrobial resistance genes (ARGs) carried by the Chinese isolates were aph(3′)-IIa, bla CTX-M-55, and bla TEM-1B, whereas bla TEM-1B, sul1, sul2, drfA7, aph(3")-Ib/strA, and aph(6)-Id/strB were most often identified in those from Africa (clade III). Among the 14 plasmid types identified, IncX1 and IncFII(pHN7A8) were found exclusively in the Chinese MDR isolates, while IncQ1 was highly associated with the African MDR isolates. The spvRABCD virulence operon was present in 94.9% (187/197) of isolates tested and was highly associated with both the IncF (IncFII and IncFIB) plasmids. In addition, phylogenetic differences in distribution of Salmonella pathogenicity islands (SPIs), prophages and other accessory genes were also noted. Taken together, these findings provide new insights into the molecular mechanisms underpinning diversification of MDR S. Enteritidis. |
| first_indexed | 2024-04-10T19:44:10Z |
| format | Article |
| id | doaj.art-6d61134f0e2845ec9f96ff80294354d1 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-10T19:44:10Z |
| publishDate | 2023-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-6d61134f0e2845ec9f96ff80294354d12023-01-29T12:08:52ZengNature PortfolioScientific Reports2045-23222023-01-0113111310.1038/s41598-022-24150-4Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humansGuojie Cao0Shaohua Zhao1Dai Kuang2Chih-Hao Hsu3Lanlan Yin4Yan Luo5Zhao Chen6Xuebin Xu7Errol Strain8Patrick McDermott9Marc Allard10Eric Brown11Jianghong Meng12Jie Zheng13Center for Food Safety and Applied Nutrition, U.S. Food and Drug AdministrationCenter for Veterinary Medicine, U.S. Food and Drug AdministrationRuijin Hospital, School of Medicine, Shanghai Jiao Tong UniversityCenter for Veterinary Medicine, U.S. Food and Drug AdministrationCenter for Food Safety and Applied Nutrition, U.S. Food and Drug AdministrationCenter for Food Safety and Applied Nutrition, U.S. Food and Drug AdministrationJoint Institute for Food Safety and Applied Nutrition, Center for Food Safety & Security Systems, Department of Nutrition and Food Science, University of MarylandShanghai Municipal Center for Disease Control and PreventionCenter for Veterinary Medicine, U.S. Food and Drug AdministrationCenter for Veterinary Medicine, U.S. Food and Drug AdministrationCenter for Food Safety and Applied Nutrition, U.S. Food and Drug AdministrationCenter for Food Safety and Applied Nutrition, U.S. Food and Drug AdministrationJoint Institute for Food Safety and Applied Nutrition, Center for Food Safety & Security Systems, Department of Nutrition and Food Science, University of MarylandCenter for Food Safety and Applied Nutrition, U.S. Food and Drug AdministrationAbstract Multidrug-resistant (MDR) Salmonella has been a long-standing challenge in public health and food safety. The prevalence of MDR S. Enteritidis, especially isolated from humans, in China is significantly higher than those from the U.S. and other countries. A dataset of 197 S. Enteritidis genomes, including 16 sequenced clinical isolates from China and 181 downloaded genomes of human isolates from the U.S., Europe, and Africa, was analyzed for genomic diversity, virulence potential, and antimicrobial resistance (AMR). Phylogenomic analyses identified four major well-supported clades (I–IV). While AMR genotype in the majority of isolates in clades I and IV displayed as pan-susceptible, 81.8% (9/11) and 22.4% (13/58) of isolates in clades III and II were MDR, respectively. It is noted that 77% (10/13) of MDR isolates in clade II were from China. The most common antimicrobial resistance genes (ARGs) carried by the Chinese isolates were aph(3′)-IIa, bla CTX-M-55, and bla TEM-1B, whereas bla TEM-1B, sul1, sul2, drfA7, aph(3")-Ib/strA, and aph(6)-Id/strB were most often identified in those from Africa (clade III). Among the 14 plasmid types identified, IncX1 and IncFII(pHN7A8) were found exclusively in the Chinese MDR isolates, while IncQ1 was highly associated with the African MDR isolates. The spvRABCD virulence operon was present in 94.9% (187/197) of isolates tested and was highly associated with both the IncF (IncFII and IncFIB) plasmids. In addition, phylogenetic differences in distribution of Salmonella pathogenicity islands (SPIs), prophages and other accessory genes were also noted. Taken together, these findings provide new insights into the molecular mechanisms underpinning diversification of MDR S. Enteritidis.https://doi.org/10.1038/s41598-022-24150-4 |
| spellingShingle | Guojie Cao Shaohua Zhao Dai Kuang Chih-Hao Hsu Lanlan Yin Yan Luo Zhao Chen Xuebin Xu Errol Strain Patrick McDermott Marc Allard Eric Brown Jianghong Meng Jie Zheng Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans Scientific Reports |
| title | Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans |
| title_full | Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans |
| title_fullStr | Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans |
| title_full_unstemmed | Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans |
| title_short | Geography shapes the genomics and antimicrobial resistance of Salmonella enterica Serovar Enteritidis isolated from humans |
| title_sort | geography shapes the genomics and antimicrobial resistance of salmonella enterica serovar enteritidis isolated from humans |
| url | https://doi.org/10.1038/s41598-022-24150-4 |
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