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The Ubiquitous Human Skin Commensal Staphylococcus hominis Protects against Opportunistic Pathogens
Morgan M Severn1, Michael R Williams2, Ali Shahbandi3
1Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, Colorado, USA.
Abstract:
Staphylococcus hominis is frequently isolated from human skin, and we hypothesize that it may protect the cutaneous barrier from opportunistic pathogens. We determined that S. hominis makes six unique autoinducing peptide (AIP) signals that inhibit the major virulence factor accessory gene regulator (agr) quorum sensing system of Staphylococcus aureus. We solved and confirmed the structures of three novel AIP signals in conditioned medium by mass spectrometry and then validated synthetic AIP activity against all S. aureus agr classes. Synthetic AIPs also inhibited the conserved agr system in a related species, Staphylococcus epidermidis. We determined the distribution of S. hominis agr types on healthy human skin and found S. hominis agr-I and agr-II were highly represented across subjects. Further, synthetic AIP-II was protective in vivo against S. aureus-associated dermonecrotic or epicutaneous injury. Together, these findings demonstrate that a ubiquitous colonizer of human skin has a fundamentally protective role against opportunistic damage. IMPORTANCE Human skin is home to a variety of commensal bacteria, including many species of coagulase-negative staphylococci (CoNS). While it is well established that the microbiota as a whole maintains skin homeostasis and excludes pathogens (i.e., colonization resistance), relatively little is known about the unique contributions of individual CoNS species to these interactions. Staphylococcus hominis is the second most frequently isolated CoNS from healthy skin, and there is emerging evidence to suggest that it may play an important role in excluding pathogens, including Staphylococcus aureus, from colonizing or infecting the skin. Here, we identified that S. hominis makes 6 unique peptide inhibitors of the S. aureus global virulence factor regulation system (agr). Additionally, we found that one of these peptides can prevent topical or necrotic S. aureus skin injury in a mouse model. Our results demonstrate a specific and broadly protective role for this ubiquitous, yet underappreciated skin commensal.
Insights
Staphylococcus hominis produces peptide signals that inhibit Staphylococcus aureus virulence. These signals protect the skin barrier from opportunistic pathogens, demonstrating a protective role for this common skin bacterium.
Area of Science:
- Microbiology
- Immunology
- Dermatology
Background:
- The human skin microbiome plays a crucial role in maintaining skin homeostasis and preventing pathogen colonization.
- Coagulase-negative staphylococci (CoNS) are abundant skin commensals, but their specific contributions to host defense are not fully understood.
- Staphylococcus hominis is a prevalent CoNS species with potential roles in pathogen exclusion.
Purpose of the Study:
- To investigate the potential protective role of Staphylococcus hominis against opportunistic skin pathogens.
- To identify and characterize the molecules produced by S. hominis that mediate this protective effect.
- To evaluate the therapeutic potential of these molecules in preventing Staphylococcus aureus-induced skin injury.
Main Methods:
- Mass spectrometry was used to identify and confirm the structures of autoinducing peptide (AIP) signals produced by S. hominis.
- Synthetic AIPs were tested for their ability to inhibit the accessory gene regulator (agr) quorum sensing system in Staphylococcus aureus and Staphylococcus epidermidis.
- The distribution of S. hominis agr types on human skin was determined.
- In vivo studies in a mouse model were conducted to assess the protective efficacy of synthetic AIPs against S. aureus skin injury.
Main Results:
- Staphylococcus hominis produces six unique autoinducing peptide (AIP) signals.
- These novel AIPs effectively inhibit the Staphylococcus aureus agr quorum sensing system across all known agr classes.
- Synthetic AIPs also demonstrated inhibitory activity against the conserved agr system in Staphylococcus epidermidis.
- Synthetic AIP-II conferred protection against Staphylococcus aureus-induced dermonecrotic and epicutaneous injury in a mouse model.
Conclusions:
- Staphylococcus hominis produces novel AIPs that antagonize the virulence of Staphylococcus aureus and Staphylococcus epidermidis.
- These findings highlight a specific protective function for S. hominis in preventing opportunistic skin infections.
- S. hominis-derived AIPs represent a promising avenue for therapeutic strategies against S. aureus-associated skin diseases.
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