Genomic Surveillance of Vancomycin-Resistant Enterococcus faecium Reveals 
Spread of a Linear Plasmid Conferring a Nutrient Utilization Advantage

Boumasmoud, Mathilde; Dengler Haunreiter, Vanina; Schweizer, Tiziano A.; Meyer, Lilly; Chakrakodi, Bhavya; Schreiber, Peter W.; Seidl, Kati; Kühnert, Denise; Kouyos, Roger D.; Zinkernagel, Annelies S.

doi:10.1128/mbio.03771-21

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Genomic Surveillance of Vancomycin-Resistant Enterococcus faecium Reveals Spread of a Linear Plasmid Conferring a Nutrient Utilization Advantage

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Citation

Boumasmoud, M., Dengler Haunreiter, V., Schweizer, T. A., Meyer, L., Chakrakodi, B., Schreiber, P. W., et al. (2022). Genomic Surveillance of Vancomycin-Resistant Enterococcus faecium Reveals Spread of a Linear Plasmid Conferring a Nutrient Utilization Advantage. mBio, 13(2). doi:10.1128/mbio.03771-21.

Cite as: https://hdl.handle.net/21.11116/0000-000A-6FF7-4

Abstract

Healthcare-associated outbreaks of vancomycin-resistant Enterococcus
faecium (VREfm) are a worldwide problem with increasing prevalence. The genomic
plasticity of this hospital-adapted pathogen contributes to its efficient spread despite
infection control measures. Here, we aimed to identify the genomic and phenotypic
determinants of health care-associated transmission of VREfm. We assessed the
VREfm transmission networks at the tertiary-care University Hospital of Zurich (USZ)
between October 2014 and February 2018 and investigated microevolutionary dy-
namics of this pathogen. We performed whole-genome sequencing for the 69
VREfm isolates collected during this time frame and assessed the population struc-
ture and variability of the vancomycin resistance transposon. Phylogenomic analysis
allowed us to reconstruct transmission networks and to unveil external or wider
transmission networks undetectable by routine surveillance. Notably, it unveiled a
persistent clone, sampled 31 times over a 29-month period. Exploring the evolution-
ary dynamics of this clone and characterizing the phenotypic consequences revealed
the spread of a variant with decreased daptomycin susceptibility and the acquired
ability to utilize N-acetyl-galactosamine (GalNAc), one of the primary constituents of
the human gut mucins. This nutrient utilization advantage was conferred by a novel
plasmid, termed pELF_USZ, which exhibited a linear topology. This plasmid, which
was harbored by two distinct clones, was transferable by conjugation. Overall, this
work highlights the potential of combining epidemiological, functional genomic, and
evolutionary perspectives to unveil adaptation strategies of VREfm.