<i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System
<i>Salmonella</i> 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...
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| Format: | Article |
| Language: | English |
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MDPI AG
2020-04-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/8/4/576 |
| _version_ | 1797570515957710848 |
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| author | Nicole A. Lerminiaux Keith D. MacKenzie Andrew D. S. Cameron |
| author_facet | Nicole A. Lerminiaux Keith D. MacKenzie Andrew D. S. Cameron |
| author_sort | Nicole A. Lerminiaux |
| collection | DOAJ |
| description | <i>Salmonella</i> 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 <i>Salmonella</i> 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 <i>fhlA</i> and <i>mutS</i>, 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 <i>Escherichia</i> ETT2, <i>Yersinia</i> YSA, <i>Pantoea</i> PSI-2, <i>Sodalis</i> SSR2, and <i>Chromobacterium</i> 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 <i>Salmonella</i>. The <i>hilA</i>, <i>hilC</i>, and <i>hilD</i> gene promoters are the most AT-rich DNA in SPI-1, placing them under tight control by the transcriptional repressor H-NS. In all <i>Salmonella</i> 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. |
| first_indexed | 2024-03-10T20:26:38Z |
| format | Article |
| id | doaj.art-ef3b9c7dfd304556af0eade61b07210e |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T20:26:38Z |
| publishDate | 2020-04-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-ef3b9c7dfd304556af0eade61b07210e2023-11-19T21:47:04ZengMDPI AGMicroorganisms2076-26072020-04-018457610.3390/microorganisms8040576<i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion SystemNicole A. Lerminiaux0Keith D. MacKenzie1Andrew D. S. Cameron2Department of Biology, Faculty of Science, University of Regina, Regina, SK S4S 0A2, CanadaDepartment of Biology, Faculty of Science, University of Regina, Regina, SK S4S 0A2, CanadaDepartment of Biology, Faculty of Science, University of Regina, Regina, SK S4S 0A2, Canada<i>Salmonella</i> 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 <i>Salmonella</i> 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 <i>fhlA</i> and <i>mutS</i>, 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 <i>Escherichia</i> ETT2, <i>Yersinia</i> YSA, <i>Pantoea</i> PSI-2, <i>Sodalis</i> SSR2, and <i>Chromobacterium</i> 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 <i>Salmonella</i>. The <i>hilA</i>, <i>hilC</i>, and <i>hilD</i> gene promoters are the most AT-rich DNA in SPI-1, placing them under tight control by the transcriptional repressor H-NS. In all <i>Salmonella</i> 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.https://www.mdpi.com/2076-2607/8/4/576genomic islandSPI-1<i>Salmonella</i>pathogenicity islandcomparative genomicstype III secretion system |
| spellingShingle | Nicole A. Lerminiaux Keith D. MacKenzie Andrew D. S. Cameron <i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System Microorganisms genomic island SPI-1 <i>Salmonella</i> pathogenicity island comparative genomics type III secretion system |
| title | <i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System |
| title_full | <i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System |
| title_fullStr | <i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System |
| title_full_unstemmed | <i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System |
| title_short | <i>Salmonella</i> Pathogenicity Island 1 (SPI-1): The Evolution and Stabilization of a Core Genomic Type Three Secretion System |
| title_sort | i salmonella i pathogenicity island 1 spi 1 the evolution and stabilization of a core genomic type three secretion system |
| topic | genomic island SPI-1 <i>Salmonella</i> pathogenicity island comparative genomics type III secretion system |
| url | https://www.mdpi.com/2076-2607/8/4/576 |
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