Metals increase the pathogenicity of the skin microbiome

Authors

• A Stacy
• Y Belkaid

Abstract

The prominent skin commensal Staphylococcus epidermidis can defend the skin from pathogens by locally enhancing T cell-mediated immunity. Although in this context S. epidermidis is beneficial, it can also develop antibiotic resistance and cause highly recalcitrant infections. As a commensal, S. epidermidis must not only survive intrinsic, skin-produced factors but also extrinsic factors such as soaps, sunscreens, and antiperspirants. How these extrinsic factors influence its interactions with the immune system is largely unknown. The active ingredient in antiperspirants is the metal aluminum. As metals have been shown to select for antibiotic resistance, we hypothesized that antiperspirants enhance S. epidermidis antibiotic resistance. To test this hypothesis, we evolved aluminum-resistant strains of S. epidermidis under in vitro and in vivo (murine skin) settings. Supporting our hypothesis, these strains showed enhanced resistance to multiple clinically relevant antibiotics. Surprisingly, these strains also showed a shift from a commensal to pathogenic lifestyle. When introduced as a commensal (by topical application onto murine skin), aluminum-resistant S. epidermidis induced a weaker T cell response compared to the non-resistant ancestor strain. In contrast, when introduced as a pathogen (by injection into murine skin), aluminum-resistant S. epidermidis induced stronger inflammation, characterized by higher monocyte numbers. Whole-genome sequencing revealed that aluminum-resistant strains harbor mutations in enzymes that modify the bacterial cell wall. Thus, currently we are exploring whether the enhanced pathogenicity of aluminum-resistant S. epidermidis is mediated by host receptors that recognize bacterial cell wall components. These studies demonstrate how prevalent environmental triggers can harm our skin microbiome and immunity.

Scientific Focus Area: Microbiology and Infectious Diseases

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