RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence

Salmonella enterica serovar Enteritidis (S. Enteritidis; wild type (WT)) is a major cause of foodborne illness globally. The ability of this pathogen to survive stress inside and outside the host, such as encountering antimicrobial peptides and heat stress, determines the efficiency of enteric infec...

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Autores principales:	Aryashree Arunima, Sunil Kumar Swain, Shilpa Ray, Birendra Kumar Prusty, Mrutyunjay Suar
Formato:	article
Lenguaje:	EN
Publicado:	Taylor & Francis Group 2020
Materias:	salmonella enteritidis sen1538 heat stress antimicrobial peptide stress spi-1 spi-2 c57bl/6 virulence inflammation illumina hiseq4000 Infectious and parasitic diseases RC109-216
Acceso en línea:	https://doaj.org/article/f0105d5b3feb4385bffebceda01f6e82
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spelling	oai:doaj.org-article:f0105d5b3feb4385bffebceda01f6e822021-11-17T14:21:58ZRpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence2150-55942150-560810.1080/21505594.2020.1743540https://doaj.org/article/f0105d5b3feb4385bffebceda01f6e822020-12-01T00:00:00Zhttp://dx.doi.org/10.1080/21505594.2020.1743540https://doaj.org/toc/2150-5594https://doaj.org/toc/2150-5608Salmonella enterica serovar Enteritidis (S. Enteritidis; wild type (WT)) is a major cause of foodborne illness globally. The ability of this pathogen to survive stress inside and outside the host, such as encountering antimicrobial peptides and heat stress, determines the efficiency of enteric infection. These stressors concertedly trigger virulence factors encoded on Salmonella pathogenicity islands (SPIs). Although RpoS is a well-known central transcriptional stress and virulence regulator, functional information regarding the genes of the regulon is currently limited. Here, we identified SEN1538 as a conserved RpoS-regulated gene belonging to the KGG protein superfamily. We further assessed its role in pathogenic stress responses and virulence. When SEN1538 was deleted (Δ1538), the pathogen showed reduced survival during antimicrobial peptide introduction and heat stress at 55°C compared to WT. The mutant displayed 70% reduced invasion in the HCT116 colon epithelial cell line, 5-fold attenuated phagocytic survival in RAW264.7 cells, and downregulation of several SPI-1 and SPI-2 genes encoding the three secretion system apparatus and effector proteins. Δ1538 also showed decreased virulence compared to WT, demonstrated by its reduced bacterial counts in the feces, mLN, spleen, and cecum of C57BL/6 mice. Comparative transcriptomic analysis of Δ1538 against WT revealed 111 differentially regulated genes, 103 of which were downregulated (fold change ≤ −1.5, P < 0.05). The majority of these genes were in clusters for metabolism, transporters, and pathogenesis, driving pathogenic stress responses and virulence. SEN1538 is, therefore, an important virulence determinant contributing to the resilience of S. Enteritidis to stress factors during infection.Aryashree ArunimaSunil Kumar SwainShilpa RayBirendra Kumar PrustyMrutyunjay SuarTaylor & Francis Grouparticlesalmonella enteritidissen1538heat stressantimicrobial peptide stressspi-1spi-2c57bl/6virulenceinflammationillumina hiseq4000Infectious and parasitic diseasesRC109-216ENVirulence, Vol 11, Iss 1, Pp 295-314 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	salmonella enteritidis sen1538 heat stress antimicrobial peptide stress spi-1 spi-2 c57bl/6 virulence inflammation illumina hiseq4000 Infectious and parasitic diseases RC109-216
spellingShingle	salmonella enteritidis sen1538 heat stress antimicrobial peptide stress spi-1 spi-2 c57bl/6 virulence inflammation illumina hiseq4000 Infectious and parasitic diseases RC109-216 Aryashree Arunima Sunil Kumar Swain Shilpa Ray Birendra Kumar Prusty Mrutyunjay Suar RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence
description	Salmonella enterica serovar Enteritidis (S. Enteritidis; wild type (WT)) is a major cause of foodborne illness globally. The ability of this pathogen to survive stress inside and outside the host, such as encountering antimicrobial peptides and heat stress, determines the efficiency of enteric infection. These stressors concertedly trigger virulence factors encoded on Salmonella pathogenicity islands (SPIs). Although RpoS is a well-known central transcriptional stress and virulence regulator, functional information regarding the genes of the regulon is currently limited. Here, we identified SEN1538 as a conserved RpoS-regulated gene belonging to the KGG protein superfamily. We further assessed its role in pathogenic stress responses and virulence. When SEN1538 was deleted (Δ1538), the pathogen showed reduced survival during antimicrobial peptide introduction and heat stress at 55°C compared to WT. The mutant displayed 70% reduced invasion in the HCT116 colon epithelial cell line, 5-fold attenuated phagocytic survival in RAW264.7 cells, and downregulation of several SPI-1 and SPI-2 genes encoding the three secretion system apparatus and effector proteins. Δ1538 also showed decreased virulence compared to WT, demonstrated by its reduced bacterial counts in the feces, mLN, spleen, and cecum of C57BL/6 mice. Comparative transcriptomic analysis of Δ1538 against WT revealed 111 differentially regulated genes, 103 of which were downregulated (fold change ≤ −1.5, P < 0.05). The majority of these genes were in clusters for metabolism, transporters, and pathogenesis, driving pathogenic stress responses and virulence. SEN1538 is, therefore, an important virulence determinant contributing to the resilience of S. Enteritidis to stress factors during infection.
format	article
author	Aryashree Arunima Sunil Kumar Swain Shilpa Ray Birendra Kumar Prusty Mrutyunjay Suar
author_facet	Aryashree Arunima Sunil Kumar Swain Shilpa Ray Birendra Kumar Prusty Mrutyunjay Suar
author_sort	Aryashree Arunima
title	RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence
title_short	RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence
title_full	RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence
title_fullStr	RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence
title_full_unstemmed	RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence
title_sort	rpos-regulated sen1538 gene promotes resistance to stress and influences salmonella enterica serovar enteritidis virulence
publisher	Taylor & Francis Group
publishDate	2020
url	https://doaj.org/article/f0105d5b3feb4385bffebceda01f6e82
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RpoS-regulated SEN1538 gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence

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