Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White

ABSTRACT The survival mechanism of Salmonella enterica serovar Enteritidis in antibacterial egg white is not fully understood. In our lab, an egg white-resistant strain, S. Enteritidis SJTUF 10978, was identified. Cell envelope damage and osmotic stress response (separation of cell wall and inner me...

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Autores principales: Xiaozhen Huang, Xiujuan Zhou, Ben Jia, Nuo Li, Jingya Jia, Mu He, Yichen He, Xiaojie Qin, Yan Cui, Chunlei Shi, Yanhong Liu, Xianming Shi
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:e6e0390e56e449c983eec5bd0e50859d2021-11-15T15:22:05ZTranscriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White10.1128/mSphere.00700-182379-5042https://doaj.org/article/e6e0390e56e449c983eec5bd0e50859d2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00700-18https://doaj.org/toc/2379-5042ABSTRACT The survival mechanism of Salmonella enterica serovar Enteritidis in antibacterial egg white is not fully understood. In our lab, an egg white-resistant strain, S. Enteritidis SJTUF 10978, was identified. Cell envelope damage and osmotic stress response (separation of cell wall and inner membrane as well as cytoplasmic shrinkage) of this strain surviving in egg white were identified through microscopic observation. RNA-Seq analysis of the transcriptome of Salmonella survival in egg white showed that a considerable number of genes involved in DNA damage repair, alkaline pH adaptation, osmotic stress adaptation, envelope damage repair, Salmonella pathogenicity island 2 (SPI-2), iron absorption, and biotin synthesis were significantly upregulated (fold change ≥ 2) in egg white, indicating that these pathways or genes might be critical for bacterial survival. RNA-Seq results were confirmed by qRT-PCR, and the survival analysis of six gene deletion mutants confirmed their importance in the survival of bacteria in egg white. The importance of alkaline pH adaptation and envelope damage repair for Salmonella to survive in egg white were further confirmed by analysis of nhaA, cpxR, waaH, and eco deletion mutants. According to the RNA-Seq results, we propose that alkaline pH adaptation might be the cause of bacterial osmotic stress phenotype and that the synergistic effect between alkaline pH and other inhibitory factors can enhance the bacteriostatic effect of egg white. Moreover, cpxR and sigE were recognized as the central regulators that coordinate bacterial metabolism to adapt to envelope damage and alkaline pH. IMPORTANCE Salmonella enterica serovar Enteritidis is a major foodborne pathogen that causes salmonellosis mainly through contaminated chicken eggs or egg products and has been a worldwide public health threat since 1980. Frequent outbreaks of this serotype through eggs correlate significantly with its exceptional survival ability in the antibacterial egg white. Research on the survival mechanism of S. Enteritidis in egg white will help to further understand the complex and highly effective antibacterial mechanisms of egg white and lay the foundation for the development of safe and effective vaccines to prevent egg contamination by this Salmonella serotype. Key pathways and genes that were previously overlooked under bactericidal conditions were characterized as being induced in egg white, and synergistic effects between different antimicrobial factors appear to exist according to the gene expression changes. Our work provides new insights into the survival mechanism of S. Enteritidis in egg white.Xiaozhen HuangXiujuan ZhouBen JiaNuo LiJingya JiaMu HeYichen HeXiaojie QinYan CuiChunlei ShiYanhong LiuXianming ShiAmerican Society for MicrobiologyarticleDNA damage repairalkaline pH adaptationenvelope damage repairosmotic stressMicrobiologyQR1-502ENmSphere, Vol 4, Iss 1 (2019)
institution DOAJ
collection DOAJ
language EN
topic DNA damage repair
alkaline pH adaptation
envelope damage repair
osmotic stress
Microbiology
QR1-502
spellingShingle DNA damage repair
alkaline pH adaptation
envelope damage repair
osmotic stress
Microbiology
QR1-502
Xiaozhen Huang
Xiujuan Zhou
Ben Jia
Nuo Li
Jingya Jia
Mu He
Yichen He
Xiaojie Qin
Yan Cui
Chunlei Shi
Yanhong Liu
Xianming Shi
Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White
description ABSTRACT The survival mechanism of Salmonella enterica serovar Enteritidis in antibacterial egg white is not fully understood. In our lab, an egg white-resistant strain, S. Enteritidis SJTUF 10978, was identified. Cell envelope damage and osmotic stress response (separation of cell wall and inner membrane as well as cytoplasmic shrinkage) of this strain surviving in egg white were identified through microscopic observation. RNA-Seq analysis of the transcriptome of Salmonella survival in egg white showed that a considerable number of genes involved in DNA damage repair, alkaline pH adaptation, osmotic stress adaptation, envelope damage repair, Salmonella pathogenicity island 2 (SPI-2), iron absorption, and biotin synthesis were significantly upregulated (fold change ≥ 2) in egg white, indicating that these pathways or genes might be critical for bacterial survival. RNA-Seq results were confirmed by qRT-PCR, and the survival analysis of six gene deletion mutants confirmed their importance in the survival of bacteria in egg white. The importance of alkaline pH adaptation and envelope damage repair for Salmonella to survive in egg white were further confirmed by analysis of nhaA, cpxR, waaH, and eco deletion mutants. According to the RNA-Seq results, we propose that alkaline pH adaptation might be the cause of bacterial osmotic stress phenotype and that the synergistic effect between alkaline pH and other inhibitory factors can enhance the bacteriostatic effect of egg white. Moreover, cpxR and sigE were recognized as the central regulators that coordinate bacterial metabolism to adapt to envelope damage and alkaline pH. IMPORTANCE Salmonella enterica serovar Enteritidis is a major foodborne pathogen that causes salmonellosis mainly through contaminated chicken eggs or egg products and has been a worldwide public health threat since 1980. Frequent outbreaks of this serotype through eggs correlate significantly with its exceptional survival ability in the antibacterial egg white. Research on the survival mechanism of S. Enteritidis in egg white will help to further understand the complex and highly effective antibacterial mechanisms of egg white and lay the foundation for the development of safe and effective vaccines to prevent egg contamination by this Salmonella serotype. Key pathways and genes that were previously overlooked under bactericidal conditions were characterized as being induced in egg white, and synergistic effects between different antimicrobial factors appear to exist according to the gene expression changes. Our work provides new insights into the survival mechanism of S. Enteritidis in egg white.
format article
author Xiaozhen Huang
Xiujuan Zhou
Ben Jia
Nuo Li
Jingya Jia
Mu He
Yichen He
Xiaojie Qin
Yan Cui
Chunlei Shi
Yanhong Liu
Xianming Shi
author_facet Xiaozhen Huang
Xiujuan Zhou
Ben Jia
Nuo Li
Jingya Jia
Mu He
Yichen He
Xiaojie Qin
Yan Cui
Chunlei Shi
Yanhong Liu
Xianming Shi
author_sort Xiaozhen Huang
title Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White
title_short Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White
title_full Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White
title_fullStr Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White
title_full_unstemmed Transcriptional Sequencing Uncovers Survival Mechanisms of <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Enteritidis in Antibacterial Egg White
title_sort transcriptional sequencing uncovers survival mechanisms of <named-content content-type="genus-species">salmonella enterica</named-content> serovar enteritidis in antibacterial egg white
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/e6e0390e56e449c983eec5bd0e50859d
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