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Metabolites derived from bacterial isolates of the human skin microbiome inhibit Staphylococcus aureus biofilm formation

V. Le,Tetyana King,Breanna Wuerzberger,Olivia R. Bauer,Megan N Carver,T. Chan,Annabeth L Henson,Grace K Hubbard,Tamar Kopadze,C. Patterson,Sabrina M McGraw,Aidan O'Hara,Eryk J Yarkosky,Michael G. LaMontagne,Eileen M Hotze,Rosana B. R. Ferreira

Published 2025 in Microbiology spectrum

ABSTRACT

ABSTRACT The human skin microbiome is a diverse ecosystem that can help prevent infections by producing biomolecules and peptides that inhibit growth and virulence of bacterial pathogens. Staphylococcus aureus is a major human pathogen responsible for diseases that range from acute skin and soft tissue infections to life-threatening septicemia. Its ability to form biofilms is a key virulence factor contributing to its success as a pathogen as well as to its increased antimicrobial resistance. Here, we investigated the ability of bacterial skin commensals to produce molecules that inhibit S. aureus biofilm formation. Matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) identified 77 human skin microbiome bacterial isolates from Staphylococcus and Bacillus genera. Metabolites from cell-free concentrated media (CFCM) from 26 representative isolates were evaluated for their ability to inhibit biofilm formation by both methicillin-resistant (MRSA) and methicillin-sensitive (MSSA) S. aureus strains. CFCM, derived from most of the isolates, inhibited biofilm formation to varying extents but did not inhibit planktonic growth of S. aureus. Size fractionation of the CFCM of three S. epidermidis isolates indicated that they produce different bioactive molecules. Cluster analysis, based on either MALDI-TOF mass spectra or whole-genome sequencing draft genomes, did not show clear clusters associated with levels of biofilm inhibition among S. epidermidis strains. Finally, similar biosynthetic gene clusters were detected in all S. epidermidis strains analyzed. These findings indicate that several bacterial constituents of the human skin microbiome display antibiofilm in vitro activity, warranting further investigation on their potential as novel therapeutic agents. IMPORTANCE The skin is constantly exposed to the environment and consequently to numerous pathogens. The bacterial community that colonizes healthy skin is thought to play an important role in protecting us against infections. S. aureus is a leading cause of death worldwide and is frequently involved in several types of infections, including skin and soft tissue infections. Its ability to adhere to surfaces and produce biofilms is considered an important virulence factor. Here, we analyzed the activity of different species of bacteria isolated from healthy skin on S. aureus biofilm formation. We found that some species of Staphylococcus and Bacillus can reduce S. aureus biofilm formation, although a generally lower level of inhibitory activity was observed compared to S. epidermidis isolates. Among S. epidermidis isolates, strength of activity was dependent on the strain. Our data highlight the importance of mining the skin microbiome for isolates that could help combat skin pathogens. The skin is constantly exposed to the environment and consequently to numerous pathogens. The bacterial community that colonizes healthy skin is thought to play an important role in protecting us against infections. S. aureus is a leading cause of death worldwide and is frequently involved in several types of infections, including skin and soft tissue infections. Its ability to adhere to surfaces and produce biofilms is considered an important virulence factor. Here, we analyzed the activity of different species of bacteria isolated from healthy skin on S. aureus biofilm formation. We found that some species of Staphylococcus and Bacillus can reduce S. aureus biofilm formation, although a generally lower level of inhibitory activity was observed compared to S. epidermidis isolates. Among S. epidermidis isolates, strength of activity was dependent on the strain. Our data highlight the importance of mining the skin microbiome for isolates that could help combat skin pathogens.

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