Salmonella bongori provides insights into the evolution of the salmonellae

Maria Fookes, Gunnar N. Schroeder, Gemma C. Langridge, Carlos J. Blondel, Caterina Mammina, Thomas R. Connor, Helena Seth-Smith, Georgios S. Vernikos, Keith S. Robinson, Mandy Sanders, Nicola K. Petty, Robert A. Kingsley, Andreas J. Bäumler, Sean Paul Nuccio, Inés Contreras, Carlos A. Santiviago, Duncan Maskell, Paul Barrow, Tom Humphrey, Antonino NastasiMark Roberts, Gad Frankel, Julian Parkhill, Gordon Dougan, Nicholas R. Thomson

Research output: Contribution to journalArticle

87 Citations (Scopus)

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.

Original languageEnglish
Article numbere1002191
JournalPLoS Pathogens
Volume7
Issue number8
DOIs
Publication statusPublished - Aug 2011
Externally publishedYes

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

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  • Cite this

    Fookes, M., Schroeder, G. N., Langridge, G. C., Blondel, C. J., Mammina, C., Connor, T. R., Seth-Smith, H., Vernikos, G. S., Robinson, K. S., Sanders, M., Petty, N. K., Kingsley, R. A., Bäumler, A. J., Nuccio, S. P., Contreras, I., Santiviago, C. A., Maskell, D., Barrow, P., Humphrey, T., ... Thomson, N. R. (2011). Salmonella bongori provides insights into the evolution of the salmonellae. PLoS Pathogens, 7(8), [e1002191]. https://doi.org/10.1371/journal.ppat.1002191