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Oxygen-dependent regulation of SPI1 type three secretion system by small RNAs in Salmonella enterica serovar Typhimurium.
Mol Microbiol. 2019 03; 111(3):570-587.MM

Abstract

Salmonella Typhimurium induces inflammatory diarrhea and uptake into intestinal epithelial cells using the Salmonella pathogenicity island 1 (SPI1) type III secretion system (T3SS). Three AraC-like regulators, HilD, HilC and RtsA, form a feed-forward regulatory loop that activates transcription of hilA, encoding the activator of the T3SS structural genes. Many environmental signals and regulatory systems are integrated into this circuit to precisely regulate SPI1 expression. A subset of these regulatory factors affects translation of hilD, but the mechanisms are poorly understood. Here, we identified two sRNAs, FnrS and ArcZ, which repress hilD translation, leading to decreased production of HilA. FnrS and ArcZ are oppositely regulated in response to oxygen, one of the key environmental signals affecting expression of SPI1. Mutational analysis demonstrates that FnrS and ArcZ bind to the hilD mRNA 5' UTR, resulting in translational repression. Deletion of fnrS led to increased HilD production under low-aeration conditions, whereas deletion of arcZ abolished the regulatory effect on hilD translation aerobically. The fnrS arcZ double mutant has phenotypes in a mouse oral infection model consistent with increased expression of SPI1. Together, these results suggest that coordinated regulation by these two sRNAs maximizes HilD production at an intermediate level of oxygen.

Authors+Show Affiliations

Department of Microbiology, University of Illinois at Urbana-Champaign, 601 S. Goodwin Ave, Urbana, IL, 61801, USA.Department of Microbiology, University of Illinois at Urbana-Champaign, 601 S. Goodwin Ave, Urbana, IL, 61801, USA.Department of Microbiology, University of Illinois at Urbana-Champaign, 601 S. Goodwin Ave, Urbana, IL, 61801, USA.Department of Microbiology, University of Illinois at Urbana-Champaign, 601 S. Goodwin Ave, Urbana, IL, 61801, USA.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

30484918

Citation

Kim, Kyungsub, et al. "Oxygen-dependent Regulation of SPI1 Type Three Secretion System By Small RNAs in Salmonella Enterica Serovar Typhimurium." Molecular Microbiology, vol. 111, no. 3, 2019, pp. 570-587.
Kim K, Golubeva YA, Vanderpool CK, et al. Oxygen-dependent regulation of SPI1 type three secretion system by small RNAs in Salmonella enterica serovar Typhimurium. Mol Microbiol. 2019;111(3):570-587.
Kim, K., Golubeva, Y. A., Vanderpool, C. K., & Slauch, J. M. (2019). Oxygen-dependent regulation of SPI1 type three secretion system by small RNAs in Salmonella enterica serovar Typhimurium. Molecular Microbiology, 111(3), 570-587. https://doi.org/10.1111/mmi.14174
Kim K, et al. Oxygen-dependent Regulation of SPI1 Type Three Secretion System By Small RNAs in Salmonella Enterica Serovar Typhimurium. Mol Microbiol. 2019;111(3):570-587. PubMed PMID: 30484918.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Oxygen-dependent regulation of SPI1 type three secretion system by small RNAs in Salmonella enterica serovar Typhimurium. AU - Kim,Kyungsub, AU - Golubeva,Yekaterina A, AU - Vanderpool,Carin K, AU - Slauch,James M, Y1 - 2018/12/12/ PY - 2018/11/22/accepted PY - 2018/11/30/pubmed PY - 2019/8/3/medline PY - 2018/11/29/entrez SP - 570 EP - 587 JF - Molecular microbiology JO - Mol Microbiol VL - 111 IS - 3 N2 - Salmonella Typhimurium induces inflammatory diarrhea and uptake into intestinal epithelial cells using the Salmonella pathogenicity island 1 (SPI1) type III secretion system (T3SS). Three AraC-like regulators, HilD, HilC and RtsA, form a feed-forward regulatory loop that activates transcription of hilA, encoding the activator of the T3SS structural genes. Many environmental signals and regulatory systems are integrated into this circuit to precisely regulate SPI1 expression. A subset of these regulatory factors affects translation of hilD, but the mechanisms are poorly understood. Here, we identified two sRNAs, FnrS and ArcZ, which repress hilD translation, leading to decreased production of HilA. FnrS and ArcZ are oppositely regulated in response to oxygen, one of the key environmental signals affecting expression of SPI1. Mutational analysis demonstrates that FnrS and ArcZ bind to the hilD mRNA 5' UTR, resulting in translational repression. Deletion of fnrS led to increased HilD production under low-aeration conditions, whereas deletion of arcZ abolished the regulatory effect on hilD translation aerobically. The fnrS arcZ double mutant has phenotypes in a mouse oral infection model consistent with increased expression of SPI1. Together, these results suggest that coordinated regulation by these two sRNAs maximizes HilD production at an intermediate level of oxygen. SN - 1365-2958 UR - https://www.unboundmedicine.com/medline/citation/30484918/Oxygen_dependent_regulation_of_SPI1_type_three_secretion_system_by_small_RNAs_in_Salmonella_enterica_serovar_Typhimurium_ DB - PRIME DP - Unbound Medicine ER -