The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis
Contribution of food vehicles to pathogenicity of disease-causing microorganisms is an important but overlooked research field. The current study was initiated to reveal the relationship between virulence of Salmonella enterica serovar Enteritidis and egg yolk as a hosting medium. Mice were orally c...
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| Format: | Article |
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2022.903979/full |
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| author | Yumin Xu Ahmed G. Abdelhamid Ahmed G. Abdelhamid Anice Sabag-Daigle Michael G. Sovic Brian M.M. Ahmer Ahmed E. Yousef Ahmed E. Yousef |
| author_facet | Yumin Xu Ahmed G. Abdelhamid Ahmed G. Abdelhamid Anice Sabag-Daigle Michael G. Sovic Brian M.M. Ahmer Ahmed E. Yousef Ahmed E. Yousef |
| author_sort | Yumin Xu |
| collection | DOAJ |
| description | Contribution of food vehicles to pathogenicity of disease-causing microorganisms is an important but overlooked research field. The current study was initiated to reveal the relationship between virulence of Salmonella enterica serovar Enteritidis and egg yolk as a hosting medium. Mice were orally challenged with Salmonella Enteritidis cultured in egg yolk or tryptic soy broth (TSB). Additionally, mice were challenged with Salmonella Enteritidis cultured in TSB, followed by administration of sterile egg yolk, to discern the difference between pre-growth of the pathogen and its mere presence in egg yolk during infection. The pathogen’s Lethal dose 50 (LD50) was the lowest when grown in yolk (2.8×102 CFU), compared to 1.1×103 CFU in TSB, and 4.6×103 CFU in TSB followed by administration of sterile yolk. Additionally, mice that orally received Salmonella Enteritidis grown in egg yolk expressed a high death rate. These findings were supported by transcriptional analysis results. Expression of promoters of virulence-related genes (sopB and sseA) in genetically modified Salmonella Enteritidis reporter strains was significantly higher (p < 0.05) when the bacterium was grown in the yolk, compared to that grown in TSB. Sequencing of RNA (RNA-seq) revealed 204 differentially transcribed genes in Salmonella Enteritidis grown in yolk vs. TSB. Yolk-grown Salmonella Enteritidis exhibited upregulated virulence pathways, including type III secretion systems, epithelial cell invasion, and infection processes; these observations were confirmed by RT-qPCR results. The transcriptomic analysis suggested that upregulation of virulence machinery of Salmonella Enteritidis grown in egg yolk was related to increased iron uptake, biotin utilization, flagellar biosynthesis, and export of virulence proteins encoded on Salmonella pathogenicity island 1, 2, 4, and 5. These biological responses may have acted in concert to increase the virulence of Salmonella infection in mice. In conclusion, growth in egg yolk enhanced Salmonella Enteritidis virulence, indicating the significance of this food vehicle to the risk assessment of salmonellosis. |
| first_indexed | 2024-12-12T07:57:46Z |
| format | Article |
| id | doaj.art-7ca60809ecf64d699a88eb00fad71987 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-12-12T07:57:46Z |
| publishDate | 2022-06-01 |
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| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-7ca60809ecf64d699a88eb00fad719872022-12-22T00:32:16ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-06-011210.3389/fcimb.2022.903979903979The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar EnteritidisYumin Xu0Ahmed G. Abdelhamid1Ahmed G. Abdelhamid2Anice Sabag-Daigle3Michael G. Sovic4Brian M.M. Ahmer5Ahmed E. Yousef6Ahmed E. Yousef7Department of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesBotany and Microbiology Department, Faculty of Science, Benha University, Benha, EgyptDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, OH, United StatesCenter for Applied Plant Sciences, The Ohio State University, Columbus, OH, United StatesDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, OH, United StatesDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesDepartment of Microbiology, The Ohio State University, Columbus, OH, United StatesContribution of food vehicles to pathogenicity of disease-causing microorganisms is an important but overlooked research field. The current study was initiated to reveal the relationship between virulence of Salmonella enterica serovar Enteritidis and egg yolk as a hosting medium. Mice were orally challenged with Salmonella Enteritidis cultured in egg yolk or tryptic soy broth (TSB). Additionally, mice were challenged with Salmonella Enteritidis cultured in TSB, followed by administration of sterile egg yolk, to discern the difference between pre-growth of the pathogen and its mere presence in egg yolk during infection. The pathogen’s Lethal dose 50 (LD50) was the lowest when grown in yolk (2.8×102 CFU), compared to 1.1×103 CFU in TSB, and 4.6×103 CFU in TSB followed by administration of sterile yolk. Additionally, mice that orally received Salmonella Enteritidis grown in egg yolk expressed a high death rate. These findings were supported by transcriptional analysis results. Expression of promoters of virulence-related genes (sopB and sseA) in genetically modified Salmonella Enteritidis reporter strains was significantly higher (p < 0.05) when the bacterium was grown in the yolk, compared to that grown in TSB. Sequencing of RNA (RNA-seq) revealed 204 differentially transcribed genes in Salmonella Enteritidis grown in yolk vs. TSB. Yolk-grown Salmonella Enteritidis exhibited upregulated virulence pathways, including type III secretion systems, epithelial cell invasion, and infection processes; these observations were confirmed by RT-qPCR results. The transcriptomic analysis suggested that upregulation of virulence machinery of Salmonella Enteritidis grown in egg yolk was related to increased iron uptake, biotin utilization, flagellar biosynthesis, and export of virulence proteins encoded on Salmonella pathogenicity island 1, 2, 4, and 5. These biological responses may have acted in concert to increase the virulence of Salmonella infection in mice. In conclusion, growth in egg yolk enhanced Salmonella Enteritidis virulence, indicating the significance of this food vehicle to the risk assessment of salmonellosis.https://www.frontiersin.org/articles/10.3389/fcimb.2022.903979/fullSalmonella Enteritidisvirulencetranscriptomic analysismouse modelstress responseRNA sequencing |
| spellingShingle | Yumin Xu Ahmed G. Abdelhamid Ahmed G. Abdelhamid Anice Sabag-Daigle Michael G. Sovic Brian M.M. Ahmer Ahmed E. Yousef Ahmed E. Yousef The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis Frontiers in Cellular and Infection Microbiology Salmonella Enteritidis virulence transcriptomic analysis mouse model stress response RNA sequencing |
| title | The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis |
| title_full | The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis |
| title_fullStr | The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis |
| title_full_unstemmed | The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis |
| title_short | The Role of Egg Yolk in Modulating the Virulence of Salmonella Enterica Serovar Enteritidis |
| title_sort | role of egg yolk in modulating the virulence of salmonella enterica serovar enteritidis |
| topic | Salmonella Enteritidis virulence transcriptomic analysis mouse model stress response RNA sequencing |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2022.903979/full |
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