Salmonella bongori provides insights into the evolution of the Salmonellae.
Schroeder, Gunnar N
Langridge, Gemma C
Blondel, Carlos J
Connor, Thomas R
Vernikos, Georgios S
Robinson, Keith S
Petty, Nicola K
Kingsley, Robert A
Bäumler, Andreas J
Santiviago, Carlos A
Thomson, Nicholas R
Public Library of Science (PLoS)
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Fookes, M., Schroeder, G. N., Langridge, G. C., Blondel, C. J., Mammina, C., Connor, T. R., Seth-Smith, H., et al. (2011). Salmonella bongori provides insights into the evolution of the Salmonellae.. PLoS Pathogens, 7 (8. e1002191)https://doi.org/10.1371/journal.ppat.1002191
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.
Animals, Biological Evolution, Enteropathogenic Escherichia coli, Genes, Bacterial, Genomic Islands, Humans, Phylogeny, Salmonella, Salmonella enterica, Sequence Analysis, DNA, Translocation, Genetic, Virulence, Virulence Factors
We thank the core sequencing and informatics teams at the Sanger Institute for their assistance and The Wellcome Trust for its support of the Sanger Institute Pathogen Genomics and Biology groups and the MRC for their support of GF, KSR and GNS. MCF, GCL, TRC, HSS, GSV, MS, NKP, RAK, JP, GD and NRT were supported by Wellcome Trust grant 076964 and MICROME, an EU Framework Programme 7 Collaborative Project, Grant Agreement Number 222886-2. Work was also supported by Grant ADI-08/2006 from Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) and The World Bank, and grant 1100092 from Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT). CJB was supported by fellowships from CONICYT (21080373 and AT-24091015).
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External DOI: https://doi.org/10.1371/journal.ppat.1002191
This record's URL: https://www.repository.cam.ac.uk/handle/1810/266009
Attribution 4.0 International
Licence URL: http://creativecommons.org/licenses/by/4.0/