A culture-based approach to study ecological interactions among the microbial species of the human scalp

Abstract

AbstractThe human scalp hosts an unusually low diversity microbiota dominated by three species:Cutibacterium acnes,Staphylococcus epidermidis, andMalassezia restricta, where characteristic shifts in species’ frequencies are associated with seborrheic dermatitis and dandruff. In order to better understand this important community, here we study the ecological interactions between these scalp species. We establish a new experimental model system that supports the growth of all three speciesin vitroand allows one to selectively enumerate each species from co-culture. Our work reveals the potential for strong ecological interactions within the scalp community. In particular,C. acnesgreatly benefits from the presence ofM. restricta, but harms it in return (exploitation), whileS. epidermidissuppresses bothM. restrictaandC. acnes. Our data suggest that the shifts in composition seen in compromised scalps are influenced by ecological interactions between species. We argue that the scalp microbiome should be viewed as an ecological system where species interactions have the potential to contribute to health outcomes.ImportanceOur bodies are home to diverse communities of microorganisms, our microbiome, which can be critical for health and wellbeing. The human scalp hosts a relatively simple community dominated by three species: two bacteria,Cutibacterium acnesandStaphylococcus epidermidis, and one fungus,Malassezia restricta. Both dandruff and seborrheic dermatitis are strongly associated with characteristic shifts in the frequencies of these three species. However, how these species affect one another and behave as a community remains poorly understood. Here, we develop a simple experimental system to empirically study how these three species interact and affect one another for the first time. We find thatS. epidermidisgreatly suppresses the growth of the other species, whileC. acnesspecifically exploitsM. restricta. Our work suggests that the human scalp is an ecological system in which species interactions have the potential to affect health outcomes.