A BTP1 prophage gene present in invasive non‐typhoidal Salmonella determines composition and length of the O‐antigen of the lipopolysaccharide

Abstract

Salmonella Typhimurium isolate D23580 represents a recently identified ST313 lineage of invasive non-typhoidal Salmonellae (iNTS). One of the differences between this lineage and other non-iNTS S. Typhimurium isolates is the presence of prophage BTP1. This prophage encodes a gtrC gene, implicated in O-antigen modification. GtrCBTP1 is essential for maintaining O-antigen length in isolate D23580, since a gtrBTP1 mutant yields a short O-antigen. This phenotype can be complemented by gtrCBTP1 or very closely related gtrC genes. The short O-antigen of the gtrBTP1 mutant was also compensated by deletion of the BTP1 phage tailspike gene in the D23580 chromosome. This tailspike protein has a putative endorhamnosidase domain and thus may mediate O-antigen cleavage. Expression of the gtrCBTP1 gene is, in contrast to expression of many other gtr operons, not subject to phase variation and transcriptional analysis suggests that gtrC is produced under a variety of conditions. Additionally, GtrCBTP1 expression is necessary and sufficient to provide protection against BTP1 phage infection of an otherwise susceptible strain. These data are consistent with a model in which GtrCBTP1 mediates modification of the BTP1 phage O-antigen receptor in lysogenic D23580, and thereby prevents superinfection by itself and other phage that uses the same O-antigen co-receptor.

Salmonella enterica Serovar Typhi Lipopolysaccharide O-Antigen Modification Impact on Serum Resistance and Antibody Recognition

“…Typhimurium (20). Additionally, we demonstrate that the family 2 gtr operon is required for the acetylation of rhamnose, as was suggested previously (21). Thus, family 2 GtrC is not a glycosyltransferase but an acyltransferase, and the gtr acronym thus reflects only proximity to (remnant) gtrAB genes (15).…”

“…Typhimurium isolate D23580. This GtrC operon has been hypothesized to acetylate the rhamnose residue of the O-antigen (21); the S . Typhi O-antigen has a rhamnose residue, but no acetylation has been described.…”

“…Rhamnose acetylation was also implicated in the strain-specific dominant epitope of the invasive S . Typhimurium D23580 isolate (33), which can be attributed to the phage-borne family 2 gtr operon that is expressed in this specific strain (21). However, detailed analyses in the context of the host, disease, and serovars are needed to further clarify the impact of O-antigen acetylation and glucosylation (36, 37).…”

“…In S. enterica serovar Typhimurium, specific modifications have been implicated in gut colonization (20) and in phage resistance (21). To better understand the extent and impact of O-antigen variation, we aimed to characterize the activity and expression of the gtr repertoire in S .…”

Bacteriophage lambda: Early pioneer and still relevant

“…These modifications change the spectrum of phages that can adsorb to the O-antigens of such lysogens and also alter the antigenicity and thus the pathogenicity of the host bacterium (Allison and Verma, 2000; Broadbent et al , 2010; Kintz et al, 2015). O-antigen modifying genes are present in two common forms in lambdoid phages.…”