Niche specialization and spread of Staphylococcus capitis involved in neonatal sepsis

Thierry Wirth (1, 2) , Marine Bergot (3) , Jean-Philippe Rasigade (1, 3, 4) , Bruno Pichon (5) , Maxime Barbier (1) , Patricia Martins-Simoes (3, 4) , Laurent Jacob (6) , Rachel Pike (5) , Pierre Tissieres (7, 8) , Jean-Charles Picaud (9) , Angela Kearns (5) , Philip Supply (10) , Marine Butin (4, 11) , Frederic Laurent (3, 4) , The International Consortium For Staphylococcus Capitis Neonatal Sepsis , The Esgs Study Group of Escmid

1 ISYEB - Institut de Systématique, Evolution, Biodiversité
2 PSL - Université Paris Sciences et Lettres
3 IAI - Institut des Agents Infectieux [Lyon]
4 CIRI - Centre International de Recherche en Infectiologie
5 Public Health England [London]
6 LBBE - Laboratoire de Biométrie et Biologie Evolutive - UMR 5558
7 I2BC - Institut de Biologie Intégrative de la Cellule
8 Hôpital Bicêtre [AP-HP, Le Kremlin-Bicêtre]
9 Hôpital de la Croix-Rousse [CHU - HCL]
10 CIIL - Centre d’Infection et d’Immunité de Lille - INSERM U 1019 - UMR 9017 - UMR 8204
11 HFME - Hôpital Femme Mère Enfant [CHU - HCL]

The multidrug-resistant Staphylococcus capitis NRCS-A clone is responsible for sepsis in preterm infants in neonatal intensive care units (NICUs) worldwide. Here, to retrace the spread of this clone and to identify drivers of its specific success, we investigated a representative collection of 250 S. capitis isolates from adults and newborns. Bayesian analyses confirmed the spread of the NRCS-A clone and enabled us to date its emergence in the late 1960s and its expansion during the 1980s, coinciding with the establishment of NICUs and the increasing use of vancomycin in these units, respectively. This dynamic was accompanied by the acquisition of mutations in antimicrobial resistance- and bacteriocin-encoding genes. Furthermore, combined statistical tools and a genome-wide association study convergently point to vancomycin resistance as a major driver of NRCS-A success. We also identified another S. capitis subclade (alpha clade) that emerged independently, showing parallel evolution towards NICU specialization and non-susceptibility to vancomycin, indicating convergent evolution in NICU-associated pathogens. These findings illustrate how the broad use of antibiotics can repeatedly lead initially commensal drug-susceptible bacteria to evolve into multidrug-resistant clones that are able to successfully spread worldwide and become pathogenic for highly vulnerable patients.

Domaines: Sciences du Vivant [q-bio]

Thierry Wirth, Marine Bergot, Jean-Philippe Rasigade, Bruno Pichon, Maxime Barbier, et al.. Niche specialization and spread of Staphylococcus capitis involved in neonatal sepsis. Nature Microbiology, 2020, 5 (5), pp.735-745. ⟨10.1038/s41564-020-0676-2⟩. ⟨hal-03056509⟩