Salmonella bongori provides insights into the evolution of the Salmonellae.
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 inf...
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2011
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oai:doaj.org-article:9e76417b94fb463d997c86aac5ce62e22021-11-18T06:03:06ZSalmonella bongori provides insights into the evolution of the Salmonellae.1553-73661553-737410.1371/journal.ppat.1002191https://doaj.org/article/9e76417b94fb463d997c86aac5ce62e22011-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21876672/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The 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.Maria FookesGunnar N SchroederGemma C LangridgeCarlos J BlondelCaterina MamminaThomas R ConnorHelena Seth-SmithGeorgios S VernikosKeith S RobinsonMandy SandersNicola K PettyRobert A KingsleyAndreas J BäumlerSean-Paul NuccioInés ContrerasCarlos A SantiviagoDuncan MaskellPaul BarrowTom HumphreyAntonino NastasiMark RobertsGad FrankelJulian ParkhillGordon DouganNicholas R ThomsonPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 7, Iss 8, p e1002191 (2011) |
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| collection |
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| topic |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 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 Nastasi Mark Roberts Gad Frankel Julian Parkhill Gordon Dougan Nicholas R Thomson Salmonella bongori provides insights into the evolution of the Salmonellae. |
| description |
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. |
| format |
article |
| author |
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 Nastasi Mark Roberts Gad Frankel Julian Parkhill Gordon Dougan Nicholas R Thomson |
| author_facet |
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 Nastasi Mark Roberts Gad Frankel Julian Parkhill Gordon Dougan Nicholas R Thomson |
| author_sort |
Maria Fookes |
| title |
Salmonella bongori provides insights into the evolution of the Salmonellae. |
| title_short |
Salmonella bongori provides insights into the evolution of the Salmonellae. |
| title_full |
Salmonella bongori provides insights into the evolution of the Salmonellae. |
| title_fullStr |
Salmonella bongori provides insights into the evolution of the Salmonellae. |
| title_full_unstemmed |
Salmonella bongori provides insights into the evolution of the Salmonellae. |
| title_sort |
salmonella bongori provides insights into the evolution of the salmonellae. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2011 |
| url |
https://doaj.org/article/9e76417b94fb463d997c86aac5ce62e2 |
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