Aerobic Cutibacterium acnes/Staphylococcus epidermidis Dual-Species Biofilms: Matrix Components In Vitro and Promotion of Cutibacterium acnes Growth on Human Skin Ex Vivo

Anaerobic Cutibacterium species and facultatively anaerobic coagulase-negative staphylococci (CoNS) are numerically abundant members of the human skin microbiota. Cutibacterium acnes can form biofilms under aerobic conditions when co-cultured with CoNS, a process that may facilitate its colonization of skin. Here, we characterized aerobic dual-species biofilms formed by C. acnes and CoNS in vitro. Aerobic growth of C. acnes in co-culture with CoNS occurred across multiple phylogenetically diverse C. acnes isolates. Moreover, C. acnes outcompeted CoNS, accounting for >90% of recovered CFUs after 5 d of aerobic co-culture. Mechanical disruption experiments showed that CoNS biofilms were readily detached by vortex agitation, whereas efficient detachment of C. acnes required sonication, suggesting stronger association with the biofilm matrix and/or culture vessel surface. All tested C. acnes strains produced detectable extracellular DNA (eDNA) and poly-N-acetylglucosamine (PNAG), and both components contributed to biofilm structural integrity and biocide resistance in aerobic dual-species biofilms. Finally, S. epidermidis supported aerobic growth of C. acnes on human skin explants ex vivo. These findings provide mechanistic insight into the ability of C. acnes to persist and dominate aerobic polymicrobial biofilms, identify eDNA and PNAG as potential targets for biofilm disruption, and suggest that cooperation with CoNS may facilitate C. acnes colonization and persistence on human skin.