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Salmonella bongori provides insights into the evolution of the Salmonellae

Fookes, Maria, Schroeder, Gunnar N., Langridge, Gemma C., Blondel, Carlos J., Mammina, Caterina, Connor, Thomas Richard ORCID: https://orcid.org/0000-0003-2394-6504, Seth-Smith, Helena, Vernikos, Georgios S., Robinson, Keith S., Sanders, Mandy, Petty, Nicola K., Kingsley, Robert A., Bäumler, Andreas J., Nuccio, Sean-Paul, Contreras, Inés, Santiviago, Carlos A., Maskell, Duncan, Barrow, Paul, Humphrey, Tom, Nastasi, Antonino, Roberts, Mark, Frankel, Gad, Parkhill, Julian, Dougan, Gordon and Thomson, Nicholas R. 2011. Salmonella bongori provides insights into the evolution of the Salmonellae. PLoS Pathogens 7 (8) , e1002191. 10.1371/journal.ppat.1002191

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Abstract

The genus Salmonella contains two species, S. bongori and S. enterica. Compared to the well-studied S. enterica there is a marked lack of information regarding the genetic makeup and diversity of S. bongori. S. bongori has been found predominantly associated with cold-blooded animals, but it can infect humans. To define the phylogeny of this species, and compare it to S. enterica, we have sequenced 28 isolates representing most of the known diversity of S. bongori. This cross-species analysis allowed us to confidently differentiate ancestral functions from those acquired following speciation, which include both metabolic and virulence-associated capacities. We show that, although S. bongori inherited a basic set of Salmonella common virulence functions, it has subsequently elaborated on this in a different direction to S. enterica. It is an established feature of S. enterica evolution that the acquisition of the type III secretion systems (T3SS-1 and T3SS-2) has been followed by the sequential acquisition of genes encoding secreted targets, termed effectors proteins. We show that this is also true of S. bongori, which has acquired an array of novel effector proteins (sboA-L). All but two of these effectors have no significant S. enterica homologues and instead are highly similar to those found in enteropathogenic Escherichia coli (EPEC). Remarkably, SboH is found to be a chimeric effector protein, encoded by a fusion of the T3SS-1 effector gene sopA and a gene highly similar to the EPEC effector nleH from enteropathogenic E. coli. We demonstrate that representatives of these new effectors are translocated and that SboH, similarly to NleH, blocks intrinsic apoptotic pathways while being targeted to the mitochondria by the SopA part of the fusion. This work suggests that S. bongori has inherited the ancestral Salmonella virulence gene set, but has adapted by incorporating virulence determinants that resemble those employed by EPEC.

Item Type: Article
Date Type: Publication
Status: Published
Schools: Biosciences
Systems Immunity Research Institute (SIURI)
Subjects: Q Science > QH Natural history > QH301 Biology
Q Science > QR Microbiology > QR180 Immunology
Publisher: Public Library of Science
ISSN: 1553-7374
Date of First Compliant Deposit: 30 March 2016
Last Modified: 10 May 2023 22:00
URI: https://orca.cardiff.ac.uk/id/eprint/41540

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