Genomic analysis of Elizabethkingia species from aquatic environments: Evidence for potential clinical transmission

Abstract

Elizabethkingia species are ubiquitous in aquatic environments, colonize water systems in healthcare settings and are emerging opportunistic pathogens with reports surfacing in 25 countries across six continents. Elizabethkingia infections are challenging to treat, and case fatality rates are high. Chromosomal bla _B , bla _GOB and bla _CME genes encoding carbapenemases and cephalosporinases are unique to Elizabethkingia spp. and reports of concomitant resistance to aminoglycosides, fluoroquinolones and sulfamethoxazole-trimethoprim are known. Here, we characterized whole-genome sequences of 94 Elizabethkingia isolates carrying multiple wide-spectrum metallo-β-lactamase (bla _B and bla _GOB) and extended-spectrum serine‑β-lactamase (bla _CME) genes from Australian aquatic environments and performed comparative phylogenomic analyses against national clinical and international strains. qPCR was performed to quantify the levels of Elizabethkingia species in the source environments. Antibiotic MIC testing revealed significant resistance to carbapenems and cephalosporins but susceptibility to fluoroquinolones, tetracyclines and trimethoprim-sulfamethoxazole. Phylogenetics show that three environmental E. anophelis isolates are closely related to E. anophelis from Australian clinical isolates (∼36 SNPs), and a new species, E. umeracha sp. novel, was discovered. Genomic signatures provide insight into potentially shared origins and a capacity to transfer mobile genetic elements with both national and international isolates.

Graphical abstract

Fig. 1

Elizabethkingia spp., E. anophelis and E. meningoseptica average absolute abundance determined by qPCR analysis of total DNA extracted from filtered waters (site A, B, C and D). Data are expressed as log10 genes copies per mL, samples (n = 32). Asterisks denote: * = P < 0.05; ** = P < 0.01.

Fig. 2

Eizabethkingia phylogeny. Mid-point rooted maximum likelihood phylogenic tree and geographic data of Elizabethkingia species using Phylosift. Samples from this collection are coloured in purple.

Fig. 3

Elizabethkingia pangenome. Pangenome analysis of 148 Elizabethkingia species from the Australian environment and clinical isolates alongside international strains.

Fig. 4

Elizabethkingia pairwise genome distances. MDS illustrating pairwise genome distances calculated using Mash. Colored by species, shapes represent isolate source. Red areas are isolates from this collection.

Fig. 5

Virulence factors of Elizabethkingia species. (A) Venn diagram of distribution of putative virulence factors across the three Elizabethkingia species identified in this collection. (B) MDS analysis of putative virulence factors identified in 148 Elizabethkingia isolates. Colored by species. Triangles = known pathogen; circles = ability to cause disease unknown. Red areas = isolates from this collection.

Fig. 6

Elizabethkiniga bla_GOB and bla_B alleles. Phylogenetic trees of all Elizabethkingia bla_B and bla_GOB alleles. Left side is the tree of bla_GOB alleles and right side is the tree of bla_B alleles. Labels are colored in red for E. miricola, green for E. anophelis, blue for E. meningoceptica and orange for E. umeracha sp. nov. Connecting space between the trees links sequences from the same isolate. Available allele numbers are presented as colored strips.