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Open AccessArticle

CRISPR-cas3 of Salmonella Upregulates Bacterial Biofilm Formation and Virulence to Host Cells by Targeting Quorum-Sensing Systems

1
The Cooperative Innovation Center for Sustainable Pig Production, Huazhong Agricultural University, Wuhan 430070, China
2
Department of Biomedical Sciences, University of North Dakota School of Medicine and Health Sciences, Grand Forks, ND 58203, USA
3
MOA Key Laboratory of Food Safety Evaluation/National Reference Laboratory of Veterinary Drug Residue (HZAU), Huazhong Agricultural University, Wuhan 430070, China
*
Authors to whom correspondence should be addressed.
Pathogens 2020, 9(1), 53; https://doi.org/10.3390/pathogens9010053
Received: 8 December 2019 / Revised: 5 January 2020 / Accepted: 7 January 2020 / Published: 10 January 2020
(This article belongs to the Special Issue Gene Regulation in Biofilms)
Salmonella is recognized as one of the most common microbial pathogens worldwide. The bacterium contains the clustered regularly interspaced short palindromic repeats (CRISPR)-CRISPR-associated (Cas) systems, providing adaptive immunity against invading foreign nucleic acids. Previous studies suggested that certain bacteria employ the Cas proteins of CRISPR-Cas systems to target their own genes, which also alters the virulence during invasion of mammals. However, whether CRISPR-Cas systems in Salmonella have similar functions during bacterial invasion of host cells remains unknown. Here, we systematically analyzed the genes that are regulated by Cas3 in a type I-E CRISPR-Cas system and the virulence changes due to the deletion of cas3 in Salmonella enterica serovar Enteritidis. Compared to the cas3 gene wild-type (cas3 WT) Salmonella strain, cas3 deletion upregulated the lsrFGBE genes in lsr (luxS regulated) operon related to quorum sensing (QS) and downregulated biofilm-forming-related genes and Salmonella pathogenicity island 1 (SPI-1) genes related to the type three secretion system (T3SS). Consistently, the biofilm formation ability was downregulated in the cas3 deletion mutant (Δcas3). The bacterial invasive and intracellular capacity of Δcas3 to host cells was also reduced, thereby increasing the survival of infected host cells and live chickens. By the transcriptome-wide screen (RNA-Seq), we found that the cas3 gene impacts a series of genes related to QS, the flagellum, and SPI-1-T3SS system, thereby altering the virulence phenotypes. As QS SPI-1-T3SS and CRISPR-Cas systems are widely distributed in the bacteria kingdom, our findings extend our understanding of virulence regulation and pathogenicity in mammalian hosts for Salmonella and potentially other bacteria. View Full-Text
Keywords: type I-E CRISPR-Cas system; cas3; Salmonella virulence; RNA-Seq; quorum sensing; biofilm formation; SPI-1-T3SS type I-E CRISPR-Cas system; cas3; Salmonella virulence; RNA-Seq; quorum sensing; biofilm formation; SPI-1-T3SS
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MDPI and ACS Style

Cui, L.; Wang, X.; Huang, D.; Zhao, Y.; Feng, J.; Lu, Q.; Pu, Q.; Wang, Y.; Cheng, G.; Wu, M.; Dai, M. CRISPR-cas3 of Salmonella Upregulates Bacterial Biofilm Formation and Virulence to Host Cells by Targeting Quorum-Sensing Systems. Pathogens 2020, 9, 53.

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