Host-Specific Evolutionary and Transmission Dynamics Shape the Functional Diversification of Staphylococcus epidermidis in Human Skin

Zhou, Wei; Spoto, Michelle; Hardy, Rachel; Guan, Changhui; Fleming, Elizabeth; Larson, Peter J.; Brown, Joseph S.; Oh, Julia

doi:10.1016/j.cell.2020.01.006

Cited by 112 publications

(169 citation statements)

References 131 publications

(185 reference statements)

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“…This may also explain why one isolate, 9 c , appeared to be phylogenetically more similar to skin isolates than the other fecal isolates. One recent study by Zhou et al (2020), reported substantial transmission of S. epidermidis strains between facial sites and other skin sites, particularly the hands and antecubital fossa, across all participants. Although no fecal samples were screened in that study, it is possible that touching of the face and mouth area may offer a route of transmission from the skin to the gut.…”

Section: Discussionmentioning

confidence: 93%

Genotypic and Phenotypic Characterization of Fecal Staphylococcus epidermidis Isolates Suggests Plasticity to Adapt to Different Human Body Sites

et al. 2020

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Staphylococcus epidermidis is a commensal species that has been increasingly identified as a nosocomial agent. Despite the interest, little is known about the ability of S. epidermidis isolates to adapt to different ecological niches through comparisons at genotype or phenotype levels. One niche where S. epidermidis has been reported is the human gut. Here, we present three S. epidermidis strains isolated from feces and show that they are not phylogenetically distinct from S. epidermidis isolated from other human body sites. Both gut and skin strains harbored multiple genes associated with biofilm formation and showed similar levels of biofilm formation on abiotic surfaces. High-throughput physiological tests using the BIOLOG technology showed no major metabolic differences between isolates from stool, skin, or cheese, while an isolate from bovine mastitis showed more phenotypic variation. Gut and skin isolates showed the ability to metabolize glycine-conjugated bile acids and to grow in the presence of bile, but the gut isolates exhibited faster anaerobic growth compared to isolates of skin origin.

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Section: Discussionmentioning

confidence: 93%

Genotypic and Phenotypic Characterization of Fecal Staphylococcus epidermidis Isolates Suggests Plasticity to Adapt to Different Human Body Sites

et al. 2020

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“…While pathogen epidemiology has long relied on comparative genomics among up to tens of thousands of isolates, it has only recently become efficient to carry out large-scale isolation of commensal organisms from human populations or individuals [170,171]. Doing so, however, opens up the ability to identify strain-level differences among isolates of the same species among individuals [12,13,172,173], within an individual microbiome at different spatial locations [81,174], or over time [170,175]. Once isolated, of course, such microbial strains can be characterized by any number of standard methods, including differences among growth curves or media, chemical (e.g., antimicrobial) resistance, metabolic flux profiling, or amplicon or shotgun sequencing.…”

Section: Strain Identification From Microbial Community Sequencingmentioning

confidence: 99%

Strain-level epidemiology of microbial communities and the human microbiome

et al. 2020

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The biological importance and varied metabolic capabilities of specific microbial strains have long been established in the scientific community. Strains have, in the past, been largely defined and characterized based on microbial isolates. However, the emergence of new technologies and techniques has enabled assessments of their ecology and phenotypes within microbial communities and the human microbiome. While it is now more obvious how pathogenic strain variants are detrimental to human health, the consequences of subtle genetic variation in the microbiome have only recently been exposed. Here, we review the operational definitions of strains (e.g., genetic and structural variants) as they can now be identified from microbial communities using different high-throughput, often culture-independent techniques. We summarize the distribution and diversity of strains across the human body and their emerging links to health maintenance, disease risk and progression, and biochemical responses to perturbations, such as diet or drugs. We list methods for identifying, quantifying, and tracking strains, utilizing highthroughput sequencing along with other molecular and "culturomics" technologies. Finally, we discuss implications of population studies in bridging experimental gaps and leading to a better understanding of the health effects of strains in the human microbiome.

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“…We postulate that S. epidermidis, through recognition of TLR2/TLR1 heterodimers on cutaneous GD T cells, regulates not only Th1 responses but also cytotoxic mediators such as P-2. The recognition of TLR2/TLR1 heterodimers may even be strain specific (12) warranting further studies on the mechanisms of P-2 induction by S. epidermidis CCN021.…”

Section: Discussionmentioning

confidence: 99%

“…One of the most common members of the healthy cutaneous microbiome is Staphylococcus epidermidis. S. epidermidis stimulates antimicrobial peptide production by skin cells (4)(5)(6)(7)(8)(9)(10)(11), which may provide protection against pathogenic bacteria (4,5,(10)(11)(12). Recent studies reported that colonization of mouse skin with S. epidermidis induced commensal-specific tissue (skin)-resident memory T cells that demonstrated immunoregulatory and tissue repair properties.…”

Section: Introductionmentioning

confidence: 99%

Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin

et al. 2020

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Perforin-2 (P-2) is an antimicrobial protein with unique properties to kill intracellular bacteria. Gamma delta (GD) T cells, as the major T cell population in epithelial tissues, play a central role in protective and pathogenic immune responses in the skin. However, the tissue-specific mechanisms that control the innate immune response and the effector functions of GD T cells, especially the cross-talk with commensal organisms, are not very well understood. We hypothesized that the most prevalent skin commensal microorganism, Staphylococcus epidermidis, may play a role in regulating GD T cellmediated cutaneous responses. We analyzed antimicrobial protein P-2 expression in human skin at a single cell resolution using an amplified fluorescence in situ hybridization approach to detect P-2 mRNA in combination with immunophenotyping. We show that S. epidermidis activates GD T cells and upregulates P-2 in human skin ex vivo in a cell-specific manner. Furthermore, P-2 upregulation following S. epidermidis stimulation correlates with increased ability of skin cells to kill intracellular Staphylococcus aureus. Our findings are the first to reveal that skin commensal bacteria induce P-2 expression, which may be utilized beneficially to modulate host innate immune responses and protect from skin infections.

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Host-Specific Evolutionary and Transmission Dynamics Shape the Functional Diversification of Staphylococcus epidermidis in Human Skin

Cited by 112 publications

References 131 publications

Genotypic and Phenotypic Characterization of Fecal Staphylococcus epidermidis Isolates Suggests Plasticity to Adapt to Different Human Body Sites

Genotypic and Phenotypic Characterization of Fecal Staphylococcus epidermidis Isolates Suggests Plasticity to Adapt to Different Human Body Sites

Strain-level epidemiology of microbial communities and the human microbiome

Staphylococcus epidermidis Boosts Innate Immune Response by Activation of Gamma Delta T Cells and Induction of Perforin-2 in Human Skin

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