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Article

Salmonella Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System

1
Department of Biology, Faculty of Science, University of Regina, Regina, SK S4S 0A2, Canada
2
Institute for Microbial Systems and Society, Faculty of Science, University of Regina, Regina, SK S4S 0A2, Canada
*
Author to whom correspondence should be addressed.
Microorganisms 2020, 8(4), 576; https://doi.org/10.3390/microorganisms8040576
Received: 5 March 2020 / Revised: 10 April 2020 / Accepted: 10 April 2020 / Published: 16 April 2020
(This article belongs to the Special Issue Salmonella: Pathogenesis and Host Restriction)
Salmonella Pathogenicity Island 1 (SPI-1) encodes a type three secretion system (T3SS), effector proteins, and associated transcription factors that together enable invasion of epithelial cells in animal intestines. The horizontal acquisition of SPI-1 by the common ancestor of all Salmonella is considered a prime example of how gene islands potentiate the emergence of new pathogens with expanded niche ranges. However, the evolutionary history of SPI-1 has attracted little attention. Here, we apply phylogenetic comparisons across the family Enterobacteriaceae to examine the history of SPI-1, improving the resolution of its boundaries and unique architecture by identifying its composite gene modules. SPI-1 is located between the core genes fhlA and mutS, a hotspot for the gain and loss of horizontally acquired genes. Despite the plasticity of this locus, SPI-1 demonstrates stable residency of many tens of millions of years in a host genome, unlike short-lived homologous T3SS and effector islands including Escherichia ETT2, Yersinia YSA, Pantoea PSI-2, Sodalis SSR2, and Chromobacterium CPI-1. SPI-1 employs a unique series of regulatory switches, starting with the dedicated transcription factors HilC and HilD, and flowing through the central SPI-1 regulator HilA. HilA is shared with other T3SS, but HilC and HilD may have their evolutionary origins in Salmonella. The hilA, hilC, and hilD gene promoters are the most AT-rich DNA in SPI-1, placing them under tight control by the transcriptional repressor H-NS. In all Salmonella lineages, these three promoters resist amelioration towards the genomic average, ensuring strong repression by H-NS. Hence, early development of a robust and well-integrated regulatory network may explain the evolutionary stability of SPI-1 compared to T3SS gene islands in other species. View Full-Text
Keywords: genomic island; SPI-1; Salmonella; pathogenicity island; comparative genomics; type III secretion system genomic island; SPI-1; Salmonella; pathogenicity island; comparative genomics; type III secretion system
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MDPI and ACS Style

Lerminiaux, N.A.; MacKenzie, K.D.; Cameron, A.D.S. Salmonella Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System. Microorganisms 2020, 8, 576. https://doi.org/10.3390/microorganisms8040576

AMA Style

Lerminiaux NA, MacKenzie KD, Cameron ADS. Salmonella Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System. Microorganisms. 2020; 8(4):576. https://doi.org/10.3390/microorganisms8040576

Chicago/Turabian Style

Lerminiaux, Nicole A., Keith D. MacKenzie, and Andrew D. S. Cameron. 2020. "Salmonella Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System" Microorganisms 8, no. 4: 576. https://doi.org/10.3390/microorganisms8040576

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