Bone cells modulate Cutibacterium acnes colonization and biofilm formation on bone and titanium

Cutibacterium acnes causes around 10 % of prosthetic joint infections, predominantly in the shoulder. Its eradication is complex due to its low virulence and its ability to form biofilm. Although C. acnes behavior on prosthetic materials like titanium is described, its interactions with bone remain poorly understood. This study investigated the impact of bone on C. acnes adhesion and biofilm formation. Two clinical strains, C2 (non-PJI) and PJI2 (PJI-isolate), were incubated with fresh (cellularized) or frozen (cell-free) bone explants, fibronectin-coated titanium discs, and combinations thereof. Adhesion and biofilm formation were assessed by colony counts, microscopies, and RT-qPCR of biofilm-related genes. Results showed that C. acnes adhered and initiated biofilm formation to bone, with upregulation of stress- and biofilm-related genes (groEL, tuf, fbaA, eno, sucD) in C2. Osteoblasts promoted C. acnes adhesion to bone, as evidenced by the reduced bacterial attachment observed on cell-free bone. The presence of bone affected C. acnes behavior on titanium: osteoblast and their secretions enhanced bacterial adhesion to titanium with an effect depending on the bacterial strain as well as the osteoblast donor. The bone mineral matrix also influenced bacterial behavior, increasing the adhesion of the PJI2 strain to the implant. However, the composition of the biofilm matrix on titanium remained unchanged. In conclusion, the bone microenvironment promotes C. acnes adhesion and biofilm formation on both bone and titanium, especially through bone cells presence. This effect strongly depends on a strain-osteoblast donor combination, highlighting the necessity of new diagnostic approach for C. acnes prosthetic joint infections.