Salmonella bongori Provides Insights into the Evolution of the Salmonellae

Fookes, María; Schroeder, Gunnar N.; Langridge, Gemma C.; Blondel, Carlos J.; Mammina, Caterina; Connor, Thomas R.; Seth-Smith, Helena M. B.; 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 J.; Barrow, Paul; Humphrey, Tom J.; Nastasi, A; Roberts, Mark; Frankel, Gad; Parkhill, Julian; Dougan, Gordon; Thomson, Nicholas R.

doi:10.1371/journal.ppat.1002191

Cited by 163 publications

(171 citation statements)

References 87 publications

(105 reference statements)

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“…S1A and Dataset S1). SL1344 shares a similar GC ratio with other S. enterica serovars, 52.3%, which is significantly higher than that of other enteric species like E. coli (19). The SL1344 genome contains 4,742 protein-coding genes (Dataset S1).…”

Section: Resultsmentioning

confidence: 95%

The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium

Kröger¹,

Dillon²,

Cameron³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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More than 50 y of research have provided great insight into the physiology, metabolism, and molecular biology of Salmonella enterica serovar Typhimurium (S. Typhimurium), but important gaps in our knowledge remain. It is clear that a precise choreography of gene expression is required for Salmonella infection, but basic genetic information such as the global locations of transcription start sites (TSSs) has been lacking. We combined three RNAsequencing techniques and two sequencing platforms to generate a robust picture of transcription in S. Typhimurium. Differential RNA sequencing identified 1,873 TSSs on the chromosome of S. Typhimurium SL1344 and 13% of these TSSs initiated antisense transcripts. Unique findings include the TSSs of the virulence regulators phoP, slyA, and invF. Chromatin immunoprecipitation revealed that RNA polymerase was bound to 70% of the TSSs, and two-thirds of these TSSs were associated with σ 70 (including phoP, slyA, and invF) from which we identified the −10 and −35 motifs of σ 70 -dependent S. Typhimurium gene promoters. Overall, we corrected the location of important genes and discovered 18 times more promoters than identified previously. S. Typhimurium expresses 140 small regulatory RNAs (sRNAs) at early stationary phase, including 60 newly identified sRNAs. Almost half of the experimentally verified sRNAs were found to be unique to the Salmonella genus, and <20% were found throughout the Enterobacteriaceae. This description of the transcriptional map of SL1344 advances our understanding of S. Typhimurium, arguably the most important bacterial infection model. transcriptional mapping | noncoding RNA | posttranscriptional regulation | pathogenicity | genome sequence

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Section: Resultsmentioning

confidence: 95%

The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium

Kröger¹,

Dillon²,

Cameron³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

370

416

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“…Evolution of pathogenicity by Salmonella is strongly associated with the acquisition of mobile genetic elements called Salmonella pathogenicity islands (SPIs). Many of these SPIs were acquired very early in the evolution of S. enterica (14), and so, perhaps unsurprisingly, their complement was found to be conserved across this entire lineage, with the exception of SPI-6 and SPI-19. Among other functions, these SPIs both encode type VI secretion systems (T6SSs), which are known to promote colonization in the avian gut (15).…”

Section: Resultsmentioning

confidence: 99%

Patterns of genome evolution that have accompanied host adaptation in Salmonella

Langridge

Fookes

Connor

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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215

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Many bacterial pathogens are specialized, infecting one or few hosts, and this is often associated with more acute disease presentation. Specific genomes show markers of this specialization, which often reflect a balance between gene acquisition and functional gene loss. Within Salmonella enterica subspecies enterica, a single lineage exists that includes human and animal pathogens adapted to cause infection in different hosts, including S. enterica serovar Enteritidis (multiple hosts), S. Gallinarum (birds), and S. Dublin (cattle). This provides an excellent evolutionary context in which differences between these pathogen genomes can be related to host range. Genome sequences were obtained from ∼60 isolates selected to represent the known diversity of this lineage. Examination and comparison of the clades within the phylogeny of this lineage revealed signs of host restriction as well as evolutionary events that mark a path to host generalism. We have identified the nature and order of events for both evolutionary trajectories. The impact of functional gene loss was predicted based upon position within metabolic pathways and confirmed with phenotyping assays. The structure of S. Enteritidis is more complex than previously known, as a second clade of S. Enteritidis was revealed that is distinct from those commonly seen to cause disease in humans or animals, and that is more closely related to S. Gallinarum. Isolates from this second clade were tested in a chick model of infection and exhibited a reduced colonization phenotype, which we postulate represents an intermediate stage in pathogen-host adaptation.Salmonella | host adaptation | pseudogene | metabolism

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“…T6SS variants have been acquired at least three times within the Salmonella lineage, and little is known about their function and mechanism, although most reports have implicated roles for the S. Typhimurium SPI-6 T6SS in the pathogenesis of mice and infection of macrophages (5,9,17,19,24,28,30,38). We found that the disruption of noncore T6SS clusters 2 and 4 caused significant defects in systemic dissemination in mice and that disruption of noncore gene clusters 1 and 3 resulted in a significant intracellular replication defect in macrophages.…”

Section: Discussionmentioning

confidence: 99%

“…arizonae, and serovars of S. enterica subsp. enterica as the most proximal element to the tRNA genes within SPI-6 or SPI-2, suggesting relatively recent acquisition events (5,17). In spite of the number of T6SS in Salmonella, an evolved VgrG effector gene has been identified only in S. enterica subsp.…”

Section: Figmentioning

confidence: 99%

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Type VI Secretion System-Associated Gene Clusters Contribute to Pathogenesis of Salmonella enterica Serovar Typhimurium

2012

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ABSTRACTThe enteropathogenSalmonella entericaserovar Typhimurium employs a suite of tightly regulated virulence factors within the intracellular compartment of phagocytic host cells resulting in systemic dissemination in mice. A type VI secretion system (T6SS) withinSalmonellapathogenicity island 6 (SPI-6) has been implicated in this process; however, the regulatory inputs and the roles of noncore genes in this system are not well understood. Here we describe four clusters of noncore T6SS genes in SPI-6 based on a comparative relationship with the T6SS-3 ofBurkholderia malleiand report that the disruption of these genes results in defects in intracellular replication and systemic dissemination in mice. In addition, we show that the expression of the SPI-6-encoded Hcp and VgrG orthologs is enhanced during late stages of macrophage infection. We identify six regions that are transcriptionally active during cell infections and that have regulatory contributions from the regulators of virulence SsrB, PhoP, and SlyA. We show that levels of protein expression are very weak underin vitroconditions and that expression is not enhanced upon the deletion ofssrB,phoP,slyA,qseC,ompR, orhfq, suggesting an unknown activating factor. These data suggest that the SPI-6 T6SS has been integrated into theSalmonellaTyphimurium virulence network and customized for host-pathogen interactions through the action of noncore genes.

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Salmonella bongori Provides Insights into the Evolution of the Salmonellae

Cited by 163 publications

References 87 publications

The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium

The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium

Patterns of genome evolution that have accompanied host adaptation in Salmonella

Type VI Secretion System-Associated Gene Clusters Contribute to Pathogenesis of Salmonella enterica Serovar Typhimurium

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