A Mixed Community of Skin Microbiome Representatives Influences Cutaneous Processes more than Individual Members

Abstract

Background Skin, the largest organ of the human body by weight, hosts a diversity of microorganisms that can influence health. The microbial residents of the skin are now appreciated for their roles in host immune interactions, wound healing, colonization resistance, and various skin disorders. Still, much remains to be discovered in terms of the host pathways influenced by skin microorganisms, as well as the higher-level skin properties impacted through these microbe-host interactions. Towards this direction, recent efforts using mouse models pointed to pronounced changes in the transcriptional profiles of the skin in response to the presence of a microbial community. However, there is a need to quantify the roles of microorganisms at both the individual and community-level in healthy human skin. In this study, we utilize human skin equivalents to study the effects of individual taxa and a microbial community in a precisely controlled context. Through transcriptomics analysis, we identify key genes and pathways influenced by skin microbes, and we also characterize higher-level impacts on skin processes and properties through histological analyses. Results The presence of a microbiome on a 3D skin tissue model led to significantly altered patterns of gene expression, influencing genes involved in the regulation of apoptosis, proliferation, and the extracellular matrix (among others). Moreover, microbiome treatment influenced the thickness of the epidermal layer, reduced the number of actively proliferating cells, and increased filaggrin expression. Many of these findings were evident upon treatment with the mixed community, but either not detected or less pronounced in treatments by single microorganisms, underscoring the impact that a diverse skin microbiome has on the host. Conclusions This work contributes to the understanding of how microbiome constituents individually and collectively influence human skin processes and properties. The results show that, while it is important to understand the effect of individual microbes on the host, a full community of microbes has unique and pronounced effects on the skin. Thus, in its impacts on the host, the skin microbiome is more than the sum of its parts.

The Role of Bifidobacteria in Predictive and Preventive Medicine: A Focus on Eczema and Hypercholesterolemia

“…Individual microorganisms elicit distinct responses in the gene expression from skin tissue. Thus, for example, Micrococcus luteus strains are able to significantly reduce epidermal thickness [ 75 ]. In vitro and in vivo model studies demonstrated the microbiota ability to increase the production of cytokines (IL-1α and IL-1β) in a tissue model [ 76 ].…”

“… Dysbiosis in atopic dermatitis and its link to the skin immune response [ 71 , 72 , 73 , 74 , 75 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 83 , 84 , 85 , 86 , 87 , 88 , 89 , 90 , 91 , 92 , 93 , 94 , 95 , 96 , 97 , 98 , 99 , 100 , 101 , 102 ]. …”

Correlation between the facial skin microbiome and sensitive skin using the 2bRAD‐M technique

“…Staphylococcus aureus is a conditional pathogen responsible for atopic dermatitis or impetigo, whereas S. epidermidis plays a key role in maintaining skin health, such as inflammation control and wound repair [10,23]. In our preliminarily study, wild-type strains isolated from the SS surface, S. capitis and M. luteus, but not S. epidermidis and S. aureus, significantly promoted IL-8 expression when treated keratinocytes for 24 h. Loomis et al [24] reported that M. luteus significantly reduced epidermal thickness and the number of proliferating cells in a 3D skin tissue model. There was little report for S. capitis on human skin.…”