Extensive variation in the O-antigen gene cluster within one Salmonella enterica serogroup reveals an unexpected complex history

Abstract

The 46 serogroups of Salmonella enterica have different O-antigens, and each is thought to have a specific form of the O-antigen cluster. Comparison of the 145 serovars of serogroup B revealed much more intraserogroup genetic diversity than expected. The O27 factor, due to an alpha 1-6 linkage between O units in place of the more common alpha 1-2 linkage and previously thought to be due to a converting bacteriophage, is now shown to be due to a wzy(alpha(1-6)) gene located within the major gene cluster. Surprisingly a remnant of this gene in all O27(-) serovars shows that the ancestor was O27(+). There are six distinct gene cluster forms, five apparently derived by a series of deletions and one by an insertion from an ancestral O27(+) form present in 57 serovars. The history of the gene cluster and movement between subspecies I and II can be traced. Two of the derivative forms still have a functional wzy(alpha(1-6)) gene, while in three it has been inactivated by deletion or insertion. Two of the forms lacking a functional wzy(alpha(1-6)) gene have the wzy(alpha(1-2)) gene first described for strain LT2 as rfc, whereas for the third the wzy gene has not been located.

FIG. 1.

Basic structure of S. enterica group B O-antigen (top) and its variants. Abbreviations: Abe, abequose; Gal, galactose; Glc, glucose; Man, mannose, OAc, O-acetyl; Rha, rhamnose.

FIG. 2.

Six different forms of S. enterica group B O-antigen gene clusters and their relationship. Positions are based on reference for the Typhimurium form and on the sequence reported in this paper for the Schleissheim form. Oligonucleotide primers are indicated by arrows. The box filled with an X indicates a remnant wzy_α(1-6) gene. Note that the wzy gene for the three O27⁻ forms except for serovar Limete is located outside of the main O-antigen gene cluster and is not shown here. The suffix -p indicates that only part of an IS element is present.