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Identification of genetic and phenotypic differences associated with prevalent and non-prevalent Salmonella Enteritidis phage types: analysis of variation in amino acid transport

Ben Carter^1,

Al Ivens^3,

¹ Department of Food and Environmental Safety, Veterinary Laboratories Agency–Weybridge, New Haw, Addlestone, Surrey KT15 3NB, UK
² School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
³ The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK

In this study, differences at the genetic level of 37 Salmonella Enteritidis strains from five phage types (PTs) were compared using comparative genomic hybridization (CGH) to assess differences between PTs. There were approximately 400 genes that differentiated prevalent (4, 6, 8 and 13a) and sporadic (11) PTs, of which 35 were unique to prevalent PTs, including six plasmid-borne genes, pefA, B, C, D, srgC and rck, and four chromosomal genes encoding putative amino acid transporters. Phenotype array studies also demonstrated that strains from prevalent PTs were less susceptible to urea stress and utilized L-histidine, L-glutamine, L-proline, L-aspartic acid, gly-asn and gly-gln more efficiently than PT11 strains. Complementation of a PT11 strain with the transporter genes from PT4 resulted in a significant increase in utilization of the amino acids and reduced susceptibility to urea stress. In epithelial cell association assays, PT11 strains were less invasive than other prevalent PTs. Most strains from prevalent PTs were better biofilm formers at 37 °C than at 28 °C, whilst the converse was true for PT11 strains. Collectively, the results indicate that genetic and corresponding phenotypic differences exist between strains of the prevalent PTs 4, 6, 8 and 13a and non-prevalent PT11 strains that are likely to provide a selective advantage for strains from the former PTs and could help them to enter the food chain and cause salmonellosis.

Correspondence
Zhensheng Pan
zhensheng{at}gmail.com

Present address: Clinical Trials and Evaluation Unit, University of Bristol, Bristol Royal Infirmary, Bristol BS2 8HW, UK.

Present address: Fios Genomics Ltd, Edinburgh Technology Transfer Centre (ETTC), King's Buildings, Edinburgh EH9 3JL, UK.

The microarray data discussed in this paper are available from ArrayExpress under accession number E-MEXP-1720.

Eight supplementary tables, listing conserved and variant genes identified from CHG microarray of 28 S. Enteritidis strains, genes identified to be unique in non-prevalent PT strains from CGH microarray, PCR validation of selected genes, MLST sequence types of 23 S. Enteritidis strains, and primers used in this study, are available with the online version of this paper.