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Salmonella Bongori Provides Insights Into the Evolution of the Salmonellae

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Salmonella Bongori Provides Insights Into the Evolution of the Salmonellae Salmonella bongori Provides Insights into the Evolution of the Salmonellae Maria Fookes1", Gunnar N. Schroeder2", Gemma C. Langridge1", Carlos J. Blondel3, Caterina Mammina4, Thomas R. Connor1, Helena Seth-Smith1, Georgios S. Vernikos1, Keith S. Robinson2, Mandy Sanders1, Nicola K. Petty1, Robert A. Kingsley1, Andreas J. Ba¨umler5, Sean-Paul Nuccio5,Ine´s Contreras3, Carlos A. Santiviago3, Duncan Maskell6, Paul Barrow7, Tom Humphrey8, Antonino Nastasi9, Mark Roberts10, Gad Frankel2, Julian Parkhill1, Gordon Dougan1, Nicholas R. Thomson1* 1 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom, 2 Centre for Molecular Microbiology and Infection, Division of Cell and Molecular Biology, Imperial College London, London, United Kingdom, 3 Departamento de Bioquı´mica y Biologı´a Molecular, Facultad de Ciencias Quı´micas y Farmace´uticas, Universidad de Chile, Santiago, Chile, 4 Dept. Sciences for Health Promotion ‘‘G. D’Alessandro’’, University of Palermo, Palermo, Italy, 5 Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, Davis, California, United State of America, 6 Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom, 7 School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Leicestershire, United Kingdom, 8 National Centre for Zoonosis Research, University of Liverpool, Leahurst Campus, Neston, Wirral, United Kingdom, 9 Dipartimento di Sanita` Publica, Universita` di Firenze, Italy, 10 Institute of Comparative Medicine, Faculty of Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom 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. Citation: Fookes M, Schroeder GN, Langridge GC, Blondel CJ, Mammina C, et al. (2011) Salmonella bongori Provides Insights into the Evolution of the Salmonellae. PLoS Pathog 7(8): e1002191. doi:10.1371/journal.ppat.1002191 Editor: Howard Ochman, Yale University, United States of America Received November 15, 2010; Accepted June 21, 2011; Published August 18, 2011 Copyright: ß 2011 Fookes et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: 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 Comisio´n Nacional de Investigacio´n Cientı´fica y Tecnolo´gica (CONICYT) and The World Bank, and grant 1100092 from Fondo Nacional de Desarrollo Cientı´fico y Tecnolo´gico (FONDECYT). CJB was supported by fellowships from CONICYT (21080373 and AT-24091015). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] " These authors have contributed equally to this manuscript and should be considered joint first. Introduction been reported to infect humans [7,8], the species is predominantly associated with cold-blooded animals whereas serovars causing Salmonella serovars are predominately pathogenic Enterobacteriaceae disease in humans and other warm-blooded animals mostly belong that are thought to have diverged from a common ancestor with to S. enterica subspecies enterica. Since S. enterica incorporates clinically Escherichia coli ,100 million years ago [1]. The genus Salmonella important pathogens, our knowledge about the genus Salmonella is currently comprises two species; S. bongori and S. enterica, with S. heavily biased and there is a marked paucity of information relating enterica being comprised of 6 subspecies enterica, salamae, arizonae, to the genetic and phylogenetic makeup of S. bongori. diarizonae, houtenae and indica [2,3,4,5,6]. These S. enterica subspecies Even though E. coli and Salmonella are estimated to have are further subdivided into .2500 serovars. Although S. bongori have diverged millions of years ago, their genomes still display PLoS Pathogens | www.plospathogens.org 1 August 2011 | Volume 7 | Issue 8 | e1002191 The Evolution of Salmonella bongori Author Summary (as described in [19]) from a selection of S. enterica Sequence types (STs) covering all of the subspecies of S. enterica. The STs for S. The bacterial genus Salmonella consists of two species: enterica were obtained from the S. enterica MLST website Salmonella enterica and Salmonella bongori. Salmonella are (mlst.ucc.ie). The S. bongori MLST gene sequences were extracted common causes of food poisoning in humans and can also from our sequenced strains (described in Table S1), and the EPEC causemoreseverediseasesuchas typhoid fever. Most of the MLST gene sequences were extracted from the genome sequence Salmonella that cause disease in humans and animals are of strain E2348/69 (Figure 1). Despite the spatial, temporal and members of S. enterica. On the other hand S. bongori, is largely phenotypic diversity described within our collection, the S. bongori associated with reptiles but can cause disease in humans, species forms a surprisingly tight cluster of sequence types (STs) albeit rarely. We have determined genomes for S. bongori clearly separated from the S. enterica subspecies (Figure 1). The S. isolates representing its known diversity. Using this, and bongori isolates in our collection fall into 20 STs, which include 11 existing genome information for a large number of different novel Salmonella STs (currently S. bongori-specific; Table S1). In members of S. enterica, we were able to identify functions comparison, there were 1,419 STs identified as being part of S. found in both species, and therefore likely to be ancestral, and rd differentiate them from those that have been more recently enterica present in the MLST database as of the 3 of May 2011. acquired. This information gives us more perspective on how To investigate the diversity and population structure of S. bongori pathogens evolve over the longer-term and allows us to we finished and fully annotated the genome of S. bongori 12419 identify functions that are associated exclusively with isolates (also known as SARC11 [20]). We then used this genome as a that commonly cause disease in humans. Our analysis reference to produce whole genome sequences for our collection of suggests that when S. bongori and S. enterica diverged they 27 further S. bongori isolates. Using the whole genome sequences we evolved to occupy very different niches. produced a phylogenetic tree using RAxML (Figure 1), following the removal of mobile genetic elements (MGE; regions excluded significant similarity including extensive regions of synteny. from this analysis are listed in Table S2). In order to determine the However, in common with other Enterobacteriaceae significant branch on which the root should be placed we also completed a diversity has been driven by horizontal gene transfer on a separate mapping including S. enterica subspecies arizonae strain background of gradual genome sequence drift [9]. Many of the CDC346-86 (S. arizonae; EMBL CP000880) strain in order to genes which are unique to Salmonella serovars,
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