Distinct clonal lineages and within-host diversification shape invasive Staphylococcus epidermidis populations

• DOI: 10.1371/journal.ppat.1009304
• Publication Date: 2021-02-08T03:56:22Z
• Authors: Anna Both; Jiabin Huang; Minyue Qi; Christian Lausmann; Samira Weißelberg; Henning Büttner; Susanne Lezius; Antonio Virgilio ...; Martin Christner; Marc Stegger; Thorsten Gehrke; Sharmin Baig; Mustafa Citak; Malik Alawi; Martin Aepfelbacher; Holger Rohde
• Keywords: Male; 0301 basic medicine; Genotype; QH301-705.5; Hemolysis; 03 medical and health sciences; Bacterial Proteins; Staphylococcus epidermidis; Humans; Biology (General); Aged; Aged, 80 and over; Cross Infection; RC581-607; Middle Aged; Staphylococcal Infections; 3. Good health; Interspersed Repetitive Sequences; Nasal Mucosa; Phenotype; Biofilms; Mutation; Female; Immunologic diseases. Allergy; Research Article

S.epidermidisis a substantial component of the human skin microbiota, but also one of the major causes of nosocomial infection in the context of implanted medical devices. We here aimed to advance the understanding ofS.epidermidisgenotypes and phenotypes conducive to infection establishment. Furthermore, we investigate the adaptation of individual clonal lines to the infection lifestyle based on the detailed analysis of individualS.epidermidispopulations of 23 patients suffering from prosthetic joint infection. Analysis of invasive and colonizingS.epidermidisprovided evidence that invasiveS.epidermidisare characterized by infection-supporting phenotypes (e.g. increased biofilm formation, growth in nutrient poor media and antibiotic resistance), as well as specific genetic traits. The discriminating gene loci were almost exclusively assigned to the mobilome. Here, in addition to IS256and SCCmec, chromosomally integrated phages was identified for the first time. These phenotypic and genotypic features were more likely present in isolates belonging to sequence type (ST) 2. By comparing seven patient-matched nasal and invasiveS.epidermidisisolates belonging to identical genetic lineages, infection-associated phenotypic and genotypic changes were documented. Besides increased biofilm production, the invasive isolates were characterized by better growth in nutrient-poor media and reduced hemolysis. By examining several colonies grown in parallel from each infection, evidence for genetic within-host population heterogeneity was obtained. Importantly, subpopulations carrying IS insertions inagrC, mutations in the acetate kinase (AckA) and deletions in the SCCmecelement emerged in several infections. In summary, these results shed light on the multifactorial processes of infection adaptation and demonstrate howS.epidermidisis able to flexibly repurpose and edit factors important for colonization to facilitate survival in hostile infection environments.