Impact of Horizontal Gene Transfer on the Evolution of Salmonella Pathogenesis

Robert A. Kingsley; Stacy M. Townsend; Tracy L. Norris; Andreas J. Bäumler; Renée M. Tsolis; Thomas A. Ficht; L. Garry Adams

doi:10.1128/9781555818111.ch15

Chapter 15 : Impact of Horizontal Gene Transfer on the Evolution of Salmonella Pathogenesis

Authors: Robert A. Kingsley¹, Stacy M. Townsend¹, Tracy L. Norris¹, Andreas J. Bäumler¹, Renée M. Tsolis², Thomas A. Ficht², L. Garry Adams²

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Affiliations: 1: Department of Medical Microbiology and Immunology, College of Medicine, Texas A&M University Health Science Center, 407 Reynolds Medical Building, College Station, TX 77843-1114; 2: Department of Veterinary Pathobiology, College of Veterinary Medicine, Texas A&M University, College Station, TX 77843-4467

Content Type: Monograph

Publication Year: 2000

Category: Bacterial Pathogenesis

Book DOI: 10.1128/9781555818111

Chapter DOI: 10.1128/9781555818111.ch15

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Abstract:

The establishment of a phylogenetic tree is a prerequisite for studying the evolution of virulence. The current nomenclature of the genus Salmonella is based on this phylogenetic tree and distinguishes only two species: Salmonella enterica and Salmonella bongori. If acquisition of SPI-1 introduced a virulence factor required for the pathogenesis of diarrheal disease, then mutational inactivation of this determinant should attenuate Salmonella serotypes in animal models of gastroenteritis. The contribution of the invasion-associated type III secretion system to serotype Typhimurium pathogenesis in this animal model has recently been investigated using strains carrying mutations in hilA and prgH. The majority of antibodies elicited by immunization with heat-killed serotype Typhimurium or with a live-attenuated serotype Typhimurium aroA vaccine is directed against the immunodominant O-antigen. Mathematical models predict that in this between-serotype competition, the serotype with higher transmissibility will dominate and eventually eliminate its competitor. The generation of O-antigen polymorphism through horizontal gene transfer was therefore a likely mechanism that allowed Salmonella serotypes to adapt to the enhanced immune memory encountered in warm-blooded hosts. The fljB gene is present in biphasic S. enterica subspecies but absent from monophasic S. enterica subspecies and Escherichia coli, suggesting its acquisition by horizontal gene transfer. A primary pathogen can be defined as an organism capable of entering a host and finding a unique niche to multiply and avoid or subvert the host defenses, the outcome of which may be clinical disease manifestations.

Citation: Kingsley R, Townsend S, Norris T, Bäumler A, Tsolis R, Ficht T, Adams L. 2000. Impact of Horizontal Gene Transfer on the Evolution of Salmonella Pathogenesis, p 227-240. In Brogden K, Roth J, Stanton T, Bolin C, Minion F, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818111.ch15

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Impact of Horizontal Gene Transfer on the Evolution of Salmonella Pathogenesis

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FIGURE 1

The evolution of dysenterylike disease. The branching structure of the phylogenetic tree shown on the left is based on comparative sequence analysis of housekeeping genes (reported previously) ( 11 ). Calibration of the phylogenetic tree of E. coli and the genus Salmonella using a molecular clock has been performed recently ( 17 , 61 ). The phylogenetic distribution of SPI-1 genes among S. bongori and S. enterica subspecies has been described by Selander and coworkers ( 48 ). Aleksic et al. reported on the ability of S. bongori and S. enterica serotypes to cause a dysenterylike disease in humans ( 2 ). The lineages in which SPI-1 and the Shigella virulence plasmid were acquired have been postulated by Ochman and Groisman and are indicated by arrows ( 59 ).

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FIGURE 1

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FIGURE 2

Evolution of systemic disease caused by Salmonella serotypes. The branching structure of the phylogenetic tree shown on the left is based on comparative sequence analysis of housekeeping genes (reported previously) ( 11 ). The phylogenetic distribution of SPI-2 has been described recently ( 31 , 58 ), suggesting its acquisition by a lineage ancestral to S. enterica (arrow). Boyd and coworkers determined the scattered phylogenetic distribution of the spv gene cluster ( 12 ). Aleksic et al. reported on the ability of S. bongori and S. enterica serotypes to cause extraintestinal infections in humans ( 2 ).

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FIGURE 2

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FIGURE 3

Adaptations of Salmonella serotypes to circulate in populations of warmblooded vertebrates. The branching structure of the phylogenetic tree shown on the left is based on comparative sequence analysis of housekeeping genes (reported previously) ( 11 ). The phylogenetic distributions of shdA and foxA have been determined recently ( 42 ; Kingsley et al., submitted). The H-antigens of monophasic and biphasic Salmonella serotypes are reviewed by Kelterborn ( 39 ). Aleksic et al. have reported on the frequency of S. bongori and S. enterica serotype isolation from clinical infections ( 2 ). a, The article by Aleksic et al. does not distinguish between S. enterica subspecies IV and VII.

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FIGURE 3

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