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

Resultado de la investigación: Article

78 Citas (Scopus)

Resumen

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.

Idioma originalEnglish
Número de artículoe1002191
PublicaciónPLoS Pathogens
Volumen7
N.º8
DOI
EstadoPublished - 1 ago 2011

Huella dactilar

Enteropathogenic Escherichia coli
Salmonella
Virulence
Genes
Proteins
Phylogeny
Mitochondria

ASJC Scopus subject areas

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

Citar esto

Fookes, M., Schroeder, G. N., Langridge, G. C., Blondel, C. J., Mammina, C., Connor, T. R., ... 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
Fookes, Maria ; Schroeder, Gunnar N. ; Langridge, Gemma C. ; Blondel, Carlos J. ; Mammina, Caterina ; Connor, Thomas R. ; 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 ; Thomson, Nicholas R. / Salmonella bongori provides insights into the evolution of the salmonellae. En: PLoS Pathogens. 2011 ; Vol. 7, N.º 8.
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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.",
author = "Maria Fookes and Schroeder, {Gunnar N.} and Langridge, {Gemma C.} and Blondel, {Carlos J.} and Caterina Mammina and Connor, {Thomas R.} and Helena Seth-Smith and Vernikos, {Georgios S.} and Robinson, {Keith S.} and Mandy Sanders and Petty, {Nicola K.} and Kingsley, {Robert A.} and B{\"a}umler, {Andreas J.} and Nuccio, {Sean Paul} and In{\'e}s Contreras and Santiviago, {Carlos A.} and Duncan Maskell and Paul Barrow and Tom Humphrey and Antonino Nastasi and Mark Roberts and Gad Frankel and Julian Parkhill and Gordon Dougan and Thomson, {Nicholas R.}",
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Fookes, M, Schroeder, GN, Langridge, GC, Blondel, CJ, Mammina, C, Connor, TR, Seth-Smith, H, Vernikos, GS, Robinson, KS, Sanders, M, Petty, NK, Kingsley, RA, Bäumler, AJ, Nuccio, SP, Contreras, I, Santiviago, CA, Maskell, D, Barrow, P, Humphrey, T, Nastasi, A, Roberts, M, Frankel, G, Parkhill, J, Dougan, G & Thomson, NR 2011, 'Salmonella bongori provides insights into the evolution of the salmonellae', PLoS Pathogens, vol. 7, n.º 8, e1002191. https://doi.org/10.1371/journal.ppat.1002191

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 R.; 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; Thomson, Nicholas R.

En: PLoS Pathogens, Vol. 7, N.º 8, e1002191, 01.08.2011.

Resultado de la investigación: Article

TY - JOUR

T1 - Salmonella bongori provides insights into the evolution of the salmonellae

AU - Fookes, Maria

AU - Schroeder, Gunnar N.

AU - Langridge, Gemma C.

AU - Blondel, Carlos J.

AU - Mammina, Caterina

AU - Connor, Thomas R.

AU - Seth-Smith, Helena

AU - Vernikos, Georgios S.

AU - Robinson, Keith S.

AU - Sanders, Mandy

AU - Petty, Nicola K.

AU - Kingsley, Robert A.

AU - Bäumler, Andreas J.

AU - Nuccio, Sean Paul

AU - Contreras, Inés

AU - Santiviago, Carlos A.

AU - Maskell, Duncan

AU - Barrow, Paul

AU - Humphrey, Tom

AU - Nastasi, Antonino

AU - Roberts, Mark

AU - Frankel, Gad

AU - Parkhill, Julian

AU - Dougan, Gordon

AU - Thomson, Nicholas R.

PY - 2011/8/1

Y1 - 2011/8/1

N2 - 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.

AB - 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.

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Fookes M, Schroeder GN, Langridge GC, Blondel CJ, Mammina C, Connor TR y otros. Salmonella bongori provides insights into the evolution of the salmonellae. PLoS Pathogens. 2011 ago 1;7(8). e1002191. https://doi.org/10.1371/journal.ppat.1002191