Distribution of Gifsy-3 and of Variants of ST64B and Gifsy-1 Prophages amongst Salmonella enterica Serovar Typhimurium Isolates: Evidence that Combinations of Prophages Promote Clonality

Abstract

Salmonella isolates harbour a range of resident prophages which can influence their virulence and ability to compete and survive in their environment. Phage gene profiling of a range of phage types of Salmonella enterica subsp. enterica serovar Typhimurium (S. Typhimurium) indicates a significant level of correlation of phage gene profile with phage type as well as correlation with genotypes determined by a combination of multi-locus variable-number tandem repeat (VNTR) typing and clustered regularly interspaced short palindromic repeats (CRISPR) typing. Variation in phage gene profiles appears to be partly linked to differences in composition of variants of known prophages. We therefore conducted a study of the distribution of variants of ST64B and Gifsy-1 prophages and coincidently the presence of Gifsy-3 prophage in a range of S. Typhimurium phage types and genotypes. We have discovered two variants of the DT104 variant of ST64B and at least two new variants of Gifsy-1 as well as variants of related phage genes. While there is definite correlation between phage type and the prophage profile based on ST64B and Gifsy-1 variants we find stronger correlation between the VNTR/CRISPR genotype and prophage profile. Further differentiation of some genotypes is obtained by addition of the distribution of Gifsy-3 and a sequence variant of the substituted SB26 gene from the DT104 variant of ST64B. To explain the correlation between genotype and prophage profile we propose that suites of resident prophages promote clonality possibly through superinfection exclusion systems.

Contributions of P2- and P22-like prophages to understanding the enormous diversity and abundance of tailed bacteriophages

“…Schmieger and co-workers (Schicklmaier et al , 1998; Schmieger, 1999) found that 173 S. enterica serovar Typhimurium isolates released a minimum of 136 functional phages, and the commonly used laboratory Typhimurium isolate LT2 carries four intact, fully functional prophages (Yamamoto, 1967 & 1969; Yamada et al , 1986; Figueroa-Bossi and Bossi, 1999; McClelland et al , 2001). Many studies have also shown that prophage content accounts for a substantial part of the natural variation among Salmonella isolates ( e.g., Reen et al , 2005; Cooke et al , 2007; Drahovska et al , 2007; Rychlik et al , 2008; Fricke et al , 2011; Moreno Switt et al , 2012; Pang et al , 2013; Bobay et al , 2014; Hiley et al , 2014; Switt et al , 2015). …”

Whole genome sequencing provides possible explanations for the difference in phage susceptibility among two Salmonella Typhimurium phage types (DT8 and DT30) associated with a single foodborne outbreak

“…Integrated prophage can block phage DNA penetration into bacterial cell as it codes blocking proteins that are localized at the membrane/cell wall level of the host cell. A strong relation between the integrated prophages and the phage type was observed [ 17 ]. For example, S. Typhimurium strain LT2 contains 4 prophages; (Fels-1, Fels-2, Gifsy-1 and Gifsy-2) [ 18 ], S. Typhimurium strain UK-1 contains 3 prophages, two that are homologous to those in LT2 (Gifsy-1, Gifsy-2) in addition to ST64B prophage [ 19 ] and S. Typhimurium strain SL1344 contains 4 prophages; 3 homologs of those in LT2 (Gifsy-1, Gifsy-2, Fels-2) and ST64B [ 20 ] and each of these strains has a distinct typing pattern as LT2, UK-1 and SL1344 strains belong to DT4, DT1 and DT44 respectively.…”

Genomic and phylogenetic analysis ofSalmonellaTyphimurium and its monophasic variants responsible for invasive endemic infections in Colombia

“…Prophages Gifsy-1 and Gifsy-2 are found in all major S. Typhimurium lineages [55] and were carried by most of the Colombian S. Typhimurium isolates (Fig. 3).…”