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Topical Antimicrobial Treatments Can Elicit Shifts to Resident Skin Bacterial Communities and Reduce Colonization by Staphylococcus aureus Competitors.

ABSTRACT: The skin microbiome is a complex ecosystem with important implications for cutaneous health and disease. Topical antibiotics and antiseptics are often employed to preserve the balance of this population and inhibit colonization by more pathogenic bacteria. However, despite their widespread use, the impact of these interventions on broader microbial communities remains poorly understood. Here, we report the longitudinal effects of topical antibiotics and antiseptics on skin bacterial communities and their role in Staphylococcus aureus colonization resistance. In response to antibiotics, cutaneous populations exhibited an immediate shift in bacterial residents, an effect that persisted for multiple days posttreatment. By contrast, antiseptics elicited only minor changes to skin bacterial populations, with few changes to the underlying microbiota. While variable in scope, both antibiotics and antiseptics were found to decrease colonization by commensal Staphylococcus spp. by sequencing- and culture-based methods, an effect which was highly dependent on baseline levels of Staphylococcus Because Staphylococcus residents have been shown to compete with the skin pathogen S. aureus, we also tested whether treatment could influence S. aureus levels at the skin surface. We found that treated mice were more susceptible to exogenous association with S. aureus and that precolonization with the same Staphylococcus residents that were previously disrupted by treatment reduced S. aureus levels by over 100-fold. In all, the results of this study indicate that antimicrobial drugs can alter skin bacterial residents and that these alterations can have critical implications for cutaneous host defense.

SUBMITTER: SanMiguel AJ

PROVIDER: S-EPMC5571303 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Topical Antimicrobial Treatments Can Elicit Shifts to Resident Skin Bacterial Communities and Reduce Colonization by Staphylococcus aureus Competitors.

SanMiguel Adam J AJ Meisel Jacquelyn S JS Horwinski Joseph J Zheng Qi Q Grice Elizabeth A EA

Antimicrobial agents and chemotherapy 20170824 9

The skin microbiome is a complex ecosystem with important implications for cutaneous health and disease. Topical antibiotics and antiseptics are often employed to preserve the balance of this population and inhibit colonization by more pathogenic bacteria. However, despite their widespread use, the impact of these interventions on broader microbial communities remains poorly understood. Here, we report the longitudinal effects of topical antibiotics and antiseptics on skin bacterial communities ...[more]

PMID: 28630195

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Project description:Staphylococcus aureus is an important pathogen responsible for nosocomial and community-acquired infections in humans, and methicillin-resistant S. aureus (MRSA) infections have continued to increase despite widespread preventative measures. S. aureus can colonize the female vaginal tract, and reports have suggested an increase in MRSA infections in pregnant and postpartum women as well as outbreaks in newborn nurseries. Currently, little is known about specific factors that promote MRSA vaginal colonization and subsequent infection. To study S. aureus colonization of the female reproductive tract in a mammalian system, we developed a mouse model of S. aureus vaginal carriage and demonstrated that both hospital-associated and community-associated MRSA isolates can colonize the murine vaginal tract. Immunohistochemical analysis revealed an increase in neutrophils in the vaginal lumen during MRSA colonization. Additionally, we observed that a mutant lacking fibrinogen binding adhesins exhibited decreased persistence within the mouse vagina. To further identify novel factors that promote vaginal colonization, we performed RNA sequencing to determine the transcriptome of MRSA growing in vivo during vaginal carriage at 5 h, 1 day, and 3 days postinoculation. Over 25% of the bacterial genes were differentially regulated at all time points during colonization compared to laboratory cultures. The most highly induced genes were those involved in iron acquisition, including the Isd system and siderophore transport systems. Mutants deficient in these pathways did not persist as well during in vivo colonization. These results reveal that fibrinogen binding and the capacity to overcome host nutritional limitation are important determinants of MRSA vaginal colonization.IMPORTANCEStaphylococcus aureus is an opportunistic pathogen able to cause a wide variety of infections in humans. Recent reports have suggested an increasing prevalence of MRSA in pregnant and postpartum women, coinciding with the increased incidence of MRSA infections in neonatal intensive care units (NICUs) and newborn nurseries. Vertical transmission from mothers to infants at delivery is a likely route of MRSA acquisition by the newborn; however, essentially nothing is known about host and bacterial factors that influence MRSA carriage in the vagina. Here, we established a mouse model of vaginal colonization and observed that multiple MRSA strains can persist in the vaginal tract. Additionally, we determined that MRSA interactions with fibrinogen and iron uptake can promote vaginal persistence. This study is the first to identify molecular mechanisms which govern vaginal colonization by MRSA, the critical initial step preceding infection and neonatal transmission.

Project description:Methicillin-resistant Staphylococcus aureus (MRSA) is an important human pathogen and often colonizes pigs. To lower the risk of MRSA transmission to humans, a reduction of MRSA prevalence and/or load in pig farms is needed. The nasal microbiome contains commensal species that may protect against MRSA colonization and may be used to develop competitive exclusion strategies. To obtain a comprehensive understanding of the species that compete with MRSA in the developing porcine nasal microbiome, and the moment of MRSA colonization, we analyzed nasal swabs from piglets in two litters. The swabs were taken longitudinally, starting directly after birth until 6 weeks. Both 16S rRNA and tuf gene sequencing data with different phylogenetic resolutions and complementary culture-based and quantitative real-time PCR (qPCR)-based MRSA quantification data were collected. We employed a compositionally aware bioinformatics approach (CoDaSeq + rmcorr) for analysis of longitudinal measurements of the nasal microbiota. The richness and diversity in the developing nasal microbiota increased over time, albeit with a reduction of Firmicutes and Actinobacteria, and an increase of Proteobacteria. Coabundant groups (CAGs) of species showing strong positive and negative correlation with colonization of MRSA and S. aureus were identified. Combining 16S rRNA and tuf gene sequencing provided greater Staphylococcus species resolution, which is necessary to inform strategies with potential protective effects against MRSA colonization in pigs. IMPORTANCE The large reservoir of methicillin-resistant Staphylococcus aureus (MRSA) in pig farms imposes a significant zoonotic risk. An effective strategy to reduce MRSA colonization in pig farms is competitive exclusion whereby MRSA colonization can be reduced by the action of competing bacterial species. We complemented 16S rRNA gene sequencing with Staphylococcus-specific tuf gene sequencing to identify species anticorrelating with MRSA colonization. This approach allowed us to elucidate microbiome dynamics and identify species that are negatively and positively associated with MRSA, potentially suggesting a route for its competitive exclusion.

Dataset Information

Topical Antimicrobial Treatments Can Elicit Shifts to Resident Skin Bacterial Communities and Reduce Colonization by Staphylococcus aureus Competitors.

Publications

Topical Antimicrobial Treatments Can Elicit Shifts to Resident Skin Bacterial Communities and Reduce Colonization by Staphylococcus aureus Competitors.

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