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.
Highlights
Bacterial genomes are highly dynamic, able to gain and lose genes over short evolutionary times
Horizontal gene transfer (HGT) disconnects the phylogenetic history of a genomic island from that of its host genome [5], which can be reflected in islands having nucleotide and codon frequencies that differ from a genomic average [6,7,8]
Many genomic island-finding programs exist [reviewed in [62,63]], but unlike other methodologies, xenoGI requires a phylogenetic tree for input
Summary
Bacterial genomes are highly dynamic, able to gain and lose genes over short evolutionary times. Gene content ranges from 3744 to 6844 open reading frames in individual E. coli isolates, only 1000 genes are shared by the over 21,000 whole genome sequences that represent this species and are currently available in GenBank [1]. As accessory genes constitute the bulk of an average bacterial genome, understanding their evolutionary histories and genetic dynamics is central to understanding bacterial functions, and capabilities. Accessory genes often become physically linked on contiguous segments of DNA, and these islands can range from two to dozens of genes. Horizontal gene transfer (HGT) is a driver of this coalescence because a physical connection between functionally linked genes increases the frequency of successful transfer [2,3,4]. Further signatures of HGT are that islands often insert adjacent to genetic elements that facilitate recombination, such as tRNA genes and mobile genetic elements [8,9,10,11]
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