Genome analysis of Salmonella enterica subsp. diarizonae isolates from invasive human infections reveals enrichment of virulence-related functions in lineage ST1256

Abstract

BackgroundSalmonella enterica subsp. diarizonae (IIIb) is frequently isolated from the environment, cold-blooded reptiles, sheep and humans; however only a few studies describe the isolation of this subspecies from invasive human infections. The factors contributing to this unusual behavior are currently unknown.ResultsWe report here the genome features of two diarizonae strains, SBO13 and SBO27, isolated from endocervical tissue collected post-abortion and from cerebrospinal fluid of a newborn child, respectively, in the city of Santa Cruz, Bolivia. Although isolated six years apart, SBO27 in 2008 and SBO13 in 2014, both strains belong to the same sequence type 1256 (ST1256) and show a high degree of genome conservation sharing more than 99% of their genes, including the conservation of a ~ 10 kb plasmid. A prominent feature of the two genomes is the presence of 24 genomic islands (GIs), in addition to 10 complete Salmonella pathogenicity islands (SPI) and fragments of SPI-7, a pathogenicity island first reported in the human-adapted serovar Typhi. Some of the GIs identified in SBO13 and SBO27 harbor genes putatively encoding auto-transporters involved in adhesion, lipopolysaccharide modifying enzymes, putative toxins, pili-related proteins, efflux pumps, and several putative membrane cation transport related-genes, among others. These two Bolivian isolates also share genes encoding the type-III secretion system effector proteins SseK2, SseK3 and SlrP with other diarizonae sequence types (ST) mainly-associated with infections in humans. The sseK2, sseK3 and slrP genes were either absent or showing frameshift mutations in a significant proportion of genomes from environmental diarizonae isolates.ConclusionsThe comparative genomic study of two diarizonae strains isolated in Bolivia from human patients uncovered the presence of many genes putatively related to virulence. The statistically-significant acquisition of a unique combination of these functions by diarizonae strains isolated from humans may have impacted the ability of these isolates to successfully infect the human host.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5352-z) contains supplementary material, which is available to authorized users.

Distinct but Intertwined Evolutionary Histories of Multiple Salmonella enterica Subspecies

“…To date, there is therefore a stark gap in sampling and genome sequencing work that has been done on non-enterica subspecies. Previous reports indicate that non-enterica subspecies have lower invasive capacity, virulence, and levels of resistance to common antibiotics, and human infections have been mostly those involving weakened immune systems (15,59). However, as we have shown in this study, there is frequent recombination between subspecies, hence these less well-known subspecies likely act as reservoirs of novel allelic variants or genes that human-associated lineages can sample from when needed (e.g., as a response to environmental change or host immune system).…”

Comparison of the phylogenetic analysis of PFGE profiles and the characteristic of virulence genes in clinical and reptile associated Salmonella strains

“…Moreover, the comparative analysis of two Salmonella diarizonae strains isolated from invasive infections of humans, revealed that this Salmonella serotype pose a huge health-risk, as Giner-Lamia et al [52] identified in genomes of S. diarizonae strains a number of genes responsible for high virulence.…”

The Not so Good, the Bad and the Ugly: Differential Bacterial Adhesion and Invasion Mediated by Salmonella PagN Allelic Variants

“…Whether other substitutions in PagN di , such as the arginine or lysine at position 150 and 154 in loop 3 (Figure 1) modulate bacterial invasion remains to be determined. Like S. Typhi, S. diarizonae have type IVB pili involved in intestinal cell invasion, raising the possibility that the concomitant increased binding property of the S. diarizonae PagN allele contributes to the reported increased bacterial virulence in humans under specific conditions [5]. Taken together, the results showed that PagN alleles with a glutamic acid residue at either 49 or 109 improves bacterial binding and/or invasiveness, possibly due to the more ionizable and long chain characteristics of glutamic acid relative to aspartic acid and glutamine.…”

“…Finally, some Salmonella such as S. enterica subsp. diarizonae (S. diarizonae) are primarily associated with cold-blooded animals, and only rarely result in invasive diseases in sheep or humans [5,6].…”