Disrupting the balance: how acne duration impacts skin microbiota assembly processes.

Abstract

Growing interest in the impact of microbial balance on health has driven studies on the ecological processes shaping the skin microbiota. Skin diseases, which alter the skin's local environment, can disrupt the microbial structure and interact with the disease itself. However, research on microbial assembly in diseased skin remains limited. In this study, we applied ecological models to characterize the processes shaping the skin microbiota in acne patients, considering the impact of disease duration on both skin pores and surfaces using bacterial amplicon sequencing. Our results revealed a significant shift in microbial diversity on the skin surface of patients with long-term acne. Further microbial community analyses showed a transition in ecological processes from healthy to diseased skin. Microbial communities on the skin surfaces of healthy controls and individuals with short-duration acne were primarily driven by heterogeneous selection, whereas microbial drift dominated the assembly process in the long-duration groups. Using the Sloan neutral model, we classified amplicon sequence variants (ASVs) into high-effect and low-effect groups based on relative abundance and sample occurrence. High-effect ASVs, likely exerting a greater ecological influence, were predominantly represented by Cutibacterium across all acne-affected skin groups, while Staphylococcus became enriched among high-effect ASVs in patients with long-term acne. Functional profiling further demonstrated that high-effect ASVs were significantly enriched in motility-related pathways. Additionally, we observed a reduction in microbial network complexity on skin surfaces as disease duration increased. Overall, the ecological dynamics of skin microbial communities may offer valuable insights into the mechanisms underlying disease onset and persistence.IMPORTANCEThe skin microbiota plays a critical role in acne development, yet the processes governing microbial assembly during acne progression remain poorly understood. Previous studies predominantly focused on factors such as acne severity, location, and duration in relation to skin microbial structure, with little attention given to the ecological mechanisms shaping the communities. In this study, we applied ecological models to investigate the processes influencing microbial assembly of skin microbiota in acne patients with varying disease durations and examined functions of ecologically important non-neutral amplicon sequence variants (ASVs). Our findings reveal a transition in ecological processes from deterministic to neutral processes as acne duration increased, with non-neutral ASVs potentially contributing to acne pathogenicity and persistence. These insights contribute to a deeper understanding of the ecological dynamics underlying acne and indicate that targeting these non-neutral ASVs or their associated functions may serve as the basis for future therapeutic strategies.