Salmonella Genomes in the Context of Lifestyle

Abstract

The Enterobacteriaceae encompass a large family of Gram‐negative gastrointestinal resident bacteria, including the Salmonella enterica species. Members of this family have persisted for millions of years, although there is diversity in terms of host range and disease phenotype. The core genome shared between all Enterobacteriaceae includes genes essential for colonising the host intestine, whereas the accessory genome that is specific to certain subspecies and serovars reflects the diversity in lifestyle. This is especially well illustrated in S. enterica, which has over 2,000 different serovars with a wide range of lifestyles, comprising generalists and host‐adapted serovars. Changes to the genome content drive this diversity and this frequently occurs via horizontal gene transfer, bacteriophage and transposon acquisition, plasmid movement and genome degradation. Many specific examples illustrate these evolutionary adaptations in Salmonella.

Key Concepts

  • Whole genome sequencing and comparative genomics have revealed a conserved ‘core genome’ common to enteric bacteria.
  • Horizontal gene transfer, bacteriophages and plasmid acquisition generates a repertoire of ‘accessory genome’ features that provides diversification.
  • Presence of certain Salmonella Pathogenicity Islands (SPIs) differentiates Salmonella from other Enterobacteriaceae and differentiates S. bongori from S. enterica: all Salmonella spp. have SPI‐1, implicated in host cell invasion, while only S. enterica has SPI‐2, which is required for survival within the host cell.
  • S. enterica is an old and complex species with over 2000 serovars that differ in terms of host range and disease phenotype.
  • S. Typhi is an example of a host‐adapted serovar that causes severe invasive disease and is restricted to humans.
  • Host adaptation in S. Typhi is driven by genome degradation, the loss of genes not required for the systemic lifestyle in human hosts and gene acquisition, including the genes encoding the Vi capsule and typhoid toxin.

Keywords: Salmonella; genomes; bacterial evolution; infectious disease; comparative genomics; genetic diversity; host adaptation

Figure 1. Phylogeny of selected members of Enterobacteriaceae based on core genes within their genomes. Coloured according to species: six subspecies of Salmonella enterica in red (S. enterica ssp. arizonae serovar 62:z36:‐ str. RKS2983, S. enterica ssp. houtenae str. ATCC BAA‐1581, S. enterica ssp. salamae str. 3588/07, S. enterica ssp. indica serovar 6,14,25:z10:1,(2),7, S. enterica ssp. enterica serovar Typhi str. CT18, S. enterica ssp. diarizonae serovar 60:r:e,n,x,z15 str. 01–0170, Salmonella bongori (S. bongori) NCTC 12419 in blue, Escherichia coli (E. coli) H10407 in green, Shigella flexneri (S. flexneri) 2a str. 301 in purple and Klebsiella pneumoniae (K. pneumoniae) ssp. pneumoniae str. HS11286 in pink. Branch lengths are indicative of the estimated substitution rate per variable site.
Figure 2. (a) Scanning EM of THP‐1 cells engulfing S. Typhimurium SL1344. (b) Cross section of S. Typhimurium SL1344 residing in the Salmonella‐containing vacuole of THP‐1 cells.
Figure 3. Phylogeny of a selection of S. enterica ssp. enterica serovars. The evolutionary relationships between 21 serovars of S. enterica (subgroup I) based on core genes within the genomes. Strains included were S. Agona str. SL483, S. Choleraesuis str. A50, S. Cubana str. CFSAN002050, S. Dublin str. 3246, S. Enteritidis str. P125109, S. Gallinarum str. 287/91, S. Heidelberg str. SL476, S. Infantis str. SARB27, S. Javiana str. CFSAN001992, S. Montevideo str. 2009083312, S. Newport str. SL254, S. Paratyphi A str. AKU 12601, S. Paratyphi B str. SPB7, S. Paratyphi C str. RKS4594, S. Pullorum str. S06004, S. Schwarzengrund str. CVM19633, S. Senftenberg str. SS209, S. Tennessee str. CDC07‐0191, S. Typhi str. Ty2, S. Typhimurium str. LT2 and S. Weltevreden str. 2007‐60‐3289‐1. Branch lengths are indicative of the estimated substitution rate per variable site.
Figure 4. Global phylogeny of S. Typhi. Mid‐rooted maximum likelihood tree of a 171 representative S. Typhi from a global collection of ∼1800 isolates. Red branches indicate the H58 lineage; reference strain S. Typhi CT18 (accession number AL513382) is highlighted on the tree; branch lengths are indicative of the estimated substitution rate per variable site.
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Further Reading

Baker S and Dougan G (2007) The genome of Salmonella enterica serovar Typhi. Clinical Infectious Diseases 45 (Supplement 1): S29–S33.

Bäumler A and Fang FC (2013) Host specificity of bacterial pathogens. Cold Spring Harbor Perspectives in Medicine 3 (12): a010041.

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Hurley D, McCusker MP, Fanning S and Martins M (2014) Salmonella‐host interactions ‐ modulation of the host innate immune system. Frontiers in Immunology 5: 481.

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Klemm, Elizabeth J, Wong, Vanessa K, and Dougan, Gordon(May 2015) Salmonella Genomes in the Context of Lifestyle. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0026130]