Genetic basis of R-phase H:z27 antigen expression and phylogenetic relationships of Salmonella enterica serovar Senftenberg

Abstract

Salmonella enterica serovar Senftenberg (S. Senftenberg) is one of the most prevalent Salmonella serovars and can be isolated from various animals and humans. According to the White-Kauffmann-Le Minor (WKL) scheme, the antigenic formula of S. Senftenberg is defined as 1,3,19:g,[s],t:-. Although the antigenic formula 1,3,19:z27:- was formerly designated as serovar Simsbury, this name was later removed from the WKL scheme due to reports of interconvertibility between serovars Senftenberg and Simsbury. The H:z27 antigen is currently recognized as one of the R-phase H antigens of S. Senftenberg. To elucidate the genetic basis of H:z27 antigen expression in S. Senftenberg, we determined the whole-genome sequences of isolates expressing the H:z27 antigen. These isolates belonged to sequence type (ST) 185 and harbored a horizontally acquired chromosomal region containing the fljA, fljB, and pinR genes, which are predicted to encode a translational repressor of fliC mRNA, a phase 2 flagellin, and an invertase, respectively. A deletion mutant lacking this region expressed the H:g,s,t antigen instead of H:z27, as confirmed by serotyping and Western blot analysis. Phylogenetic analysis based on S. Senftenberg genome archives, together with the sequences obtained in this study, suggested that the S. Senftenberg ST185 lineage acquired the fljAB-pinR locus around 1867. In contrast, our broader phylogenetic analysis of Salmonella serovars indicated that S. Senftenberg ST14 is genetically closer to certain other serovars than to ST185, while ST185 shows a closer relationship to a different serovar than to ST14. These findings suggest that S. Senftenberg comprises at least two distinct genomic lineages. IMPORTANCELimited information is available on the genetic basis of R-phase H antigen expression in S. enterica. In this study, we first demonstrated that the R-phase H:z27 antigen of S. Senftenberg is determined by a horizontally acquired chromosomal region. The ST 185 lineage of S. Senftenberg appears to have acquired this chromosomal region around 1867 and subsequently disseminated worldwide. We also demonstrated that S. Senftenberg comprises at least two distinct genomic lineages. The combined use of serotyping and multilocus sequence typing may provide a typing framework that better reflects the disease potential of Salmonella.