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

Abstract

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.

Performance of four commercial real-time PCR assays for the detection of bacterial enteric pathogens in clinical samples

“…Regarding Salmonella, all RT-PCRs had good performance and detected commonly circulating Salmonella serotypes. This was despite heterogeneity in the Salmonella targets of commercial assays, which include pathogenicity island targets (ttr (Ridagene), spaO (BD max), and orgC (Prodesse) (Lerminiaux et al, 2020;Hensel et al, 1999), indicating that they are all appropriate targets. However, our study did exemplify the need for a diversity of PCR targets tested in the diagnostic lab system at large to identify the loss of or mutations in target genes and strengthen surveillance activities.…”

Complete, closed and curated genome sequences of Photobacterium damselae subsp. piscicida isolates from Australia indicate mobilome-driven localized evolution and novel pathogenicity determinants

“…Pathogenicity islands and plasmids are well known for their ability to severely alter the phenotype and, as a result, the virulence of several bacteria. Some of them are essential to the emergence of novel or highly pathogenic strains and species that stably maintain ‘foreign’ genetic elements in their genomes, such as the type III secretion system in Salmonella pathogenicity island 1 (SPI-1) [ 48 ]. Bacteriophages also play a substantial role in the evolution and adaptation of pathogens.…”

Genomic Characterization of Salmonella enterica Isolates From Retail Meat in Beijing, China

“…The pathogenesis of Salmonella is associated with the expression of virulence-associated determinants in Salmonella pathogenicity islands (SPIs) ( Groisman and Ochman, 1996 ). To date, 24 different SPIs have been identified, but not all of them have been experimentally validated ( Lerminiaux et al, 2020 ). Two distinct type III secretion systems (TTSSs) encoded by SPI-1 and SPI-2 are considered central to the pathogenicity of NTS ( Suez et al, 2013 ).…”