(2017). (2009). A commensal strain of Staphylococcus epidermidis protects against skin neoplasia. Figure 3. (2015). Characterization of microbiome and human host from three cohorts of microbiome-associated conditions, using multiple 'omics technologies. (2011). (2017) isolated the CoNS collected from the skin of normal and AD individuals using high-throughput screening for antimicrobial activity against S. aureus. (2012). Transl. (2018). This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). 7, 555–567. JAMA Dermatol. Sci. (2016). Percentage of relative abundance of diverse C. acnes strains in the pilosebaceous units between acne patients and normal individuals. Dermatol. Small CRISPR RNAs guide antiviral defense in prokaryotes. Notably, patients with C. acnes subtype H1 and Leifsonia being more abundant showed a markedly higher transplantation by using a multistrain donor solution, suggesting that different microbiota might have a synergistic effect (Figure 4; Paetzold et al., 2019). Nature 514, 59–64. 2, 799–808. 139, S58–S64. 16, 143–155. Anaerobe 47, 57–63. Association between Staphylococcus aureus nasal carriage and disease phenotype in patients affected by systemic lupus erythematosus. The results of strain tracking were well confirmed using a complementary approach in which SNVs were identified in the 1.9 Mbp core genome shared between all sequenced S. aureus. Actually, it is still unknown how the homeostasis is maintained and shaped by the skin microbiota, but the balance between members of skin microbial communities plays a pivotal role in guarding against cutaneous disorders (Dreno et al., 2016). The skin microbiota is the term used to describe the millions of different organisms – bacteria, viruses and fungi – that live on Human Skin. HHS Transl. The human skin microbiome. The opportunistic pathogen Staphylococcus aureus asymptomatically colonizes more than 30% of the individuals under steady-state conditions in a relatively low colonization rate and barely detectable abundance levels (Totté et al., 2016; Totte et al., 2016), indicating that potentially pathogenic bacteria that colonize the skin of healthy individuals are influenced by the native microbial community. 10:570261. doi: 10.3389/fcimb.2020.570261. 9:eaah6500. The available evidence has clearly indicated that the dysbiosis of cutaneous microbiota is substantially associated with multiple skin disorders, and the degree of disorder has a positive correlation with the severity of skin disease. An increased incidence of Propionibacterium acnes biofilms in acne vulgaris: a case-control study. Allergy Clin. Lancet 379, 361–372. Dupilumab progressively improves systemic and cutaneous abnormalities in patients with atopic dermatitis. Commun. AD can persist into adulthood in certain AD children or begin in adulthood (Garmhausen et al., 2013). J. doi: 10.1126/scitranslmed.aat8329, Wu, G., Zhao, H., Li, C., Rajapakse, M. P., Wong, W. C., Xu, J., et al. Dermatol. Epidemiological trends in skin mycoses worldwide. Until recently, the diversity of the cutaneous microbiota was mainly investigated for bacteria through culture based assays subsequently confirmed by molecular techniques. 23, 2103–2114. Interspecies interactions influence the composition of microbial communities, but their mechanisms are poorly understood. Association of systemic antibiotic treatment of acne with skin microbiota characteristics. In particular, Cutibacterium acnes, the most abundant commensal (up to 90%) in the skin-residing microorganisms of healthy adults, has been viewed as an important pathogenic factor accompanying the development of AV (Melnik, 2015; Barnard et al., 2016; Lomholt et al., 2017). It is possible that heightened understanding of the communication network of skin microbiota in molecular mechanisms will contribute to the amelioration of dysbiosis and may provide more targeted therapies for dysbiosis. We would like to thank all the members of Liu Group who gave valuable suggestions on this manuscript. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. doi: 10.1038/nrmicro2182, Otto, M., Echner, H., Voelter, W., and Gotz, F. (2001). Recent advances, showing that the application of natural bacteria to the human skin modulates skin microbiota composition, underscore the importance for the manipulation in the indigenous microbiota of patients and highlight an opportunity to develop an ecology-based therapeutic modality that specifically target the invading pathogens while preserving indigenous commensal bystanders in diseases affecting the skin (Parlet et al., 2019; Stacy and Belkaid, 2019). Figure 1a presents binary traits for skin microbes. LS, YR, and XT carried out revisions of the manuscript. Recent advances in unlocking a key understanding of the cellular mechanisms through which the microbiota implement both the establishment and restoration of cutaneous homeostasis highlight three indispensable essential interactions (Figure 4): (i) antimicrobial peptides (AMPs) or other metabolites produced by reintroduction of a single of microbiota directly inhibit or kill pathogenic microorganisms (Nakatsuji et al., 2017, 2018; Williams et al., 2019); (ii) reintroduction of living microbiota induces keratinocytes and sebocytes to produce AMPs to shape microbial communities (Nagy et al., 2005, 2006; Naik et al., 2015); and (iii) reintroduction of a cocktail of microbiota has a synergistic effect on ameliorating the ecology of skin microbial communities (Paetzold et al., 2019). Functioning as the exterior interface of the human body with the environment, skin acts as a physical barrier to prevent the invasion of foreign pathogens while providing a home to the commensal microbiota. Gut 66, 569–580. 2013 Feb;8(2):209-22. doi: 10.2217/fmb.12.141. Amphibians have microbiota on their skin. Michalik M, Samet A, Podbielska-Kubera A, Savini V, Międzobrodzki J, Kosecka-Strojek M. Ann Clin Microbiol Antimicrob. (2019). Recently, Moestrup et al. doi: 10.1038/nrmicro1636, Totte, J. E., van der Feltz, W. T., Bode, L. G., van Belkum, A., van Zuuren, E. J., and Pasmans, S. G. (2016). (2013). Verhulst, Y.T. A., Earland, N. J., Anderson, E. D., Moore, I. N., Kieh, M. D., Williams, K. W., et al. doi: 10.1038/jid.2013.21, Fuller, J. D., Camus, A. C., Duncan, C. L., Nizet, V., Bast, D. J., Thune, R. L., et al. Natl. Composition of Human Skin Microbiota Affects Attractiveness to Malaria Mosquitoes. doi: 10.1038/nature25177, Chien, A. L., Tsai, J., Leung, S., Mongodin, E. F., Nelson, A. M., Kang, S., et al. Drug Discov. J. The altered landscape of the human skin microbiome in patients with primary immunodeficiencies. Mech. N. Engl. | Skin microbiome and skin disease: the example of rosacea. Cutaneous microbiome studies in the times of affordable sequencing. The human skin microbiome plays an important role in both health and disease. It is implicated in several severe skin diseases and plays a major role in wound infections. Staphylococcus aureus and atopic dermatitis: a complex and evolving relationship. Acne: transient arrest in the homeostatic host-microbiota dialog? (2015). U.S.A. 108, 6252–6257. The human skin is a complex ecosystem that hosts a heterogeneous flora. (2016). The result uncovered a more than 90% decrease in the number of S. aureus on their skin by a single application. High frequency and diversity of antimicrobial activities produced by nasal staphylococcus strains against bacterial competitors. Trait composition of the human skin microbiome. Acne: clinical presentations. doi: 10.1038/jid.2011.417, Lax, S., Sangwan, N., Smith, D., Larsen, P., Handley, K. M., Richardson, M., et al. doi: 10.1126/scitranslmed.aah4680, Neuman, H., and Koren, O. Ther 18:177. doi: 10.1186/s13075-016-1079-x, Cunliffe, W. J., and Gould, D. J. The human skin hosts a diverse community of commensal bacteria, fungi, viruses, and parasites, which collectively constitute the skin microbiota. 75, 481–493.e488. In another in vitro study, two clinical isolates of C. acnes type IA and IB significantly induced the expression of β-defensin-2 in human sebocytes and keratinocytes (Nagy et al., 2005, 2006). 35, 1069–1077. (2015). Cell Host Microbe 22, 746–756.e745. Although the etiology and pathogenesis of AV are not well-understood, multifaceted involvements encompassing androgen-induced increased sebum secretion and sebaceous gland proliferation, hypercornification of the pilosebaceous follicle, inflammation involving innate and acquired immunity response, skin microbiota colonization and proliferation in the pilosebaceous unit, and external factors and genetics are considered as the mechanisms contributing to the development of AV (Agak et al., 2018; O'Neill and Gallo, 2018; Chien et al., 2019). Prevalence of facial acne vulgaris in late adolescence and in adults. AD most often develops in early childhood, and up to 70% of AD children demonstrate clearing of the disease or a spontaneous resolution until late childhood even in patients with FLG mutations (Margolis et al., 2014; Mortz et al., 2015; Bieber et al., 2017). JAMA Dermatol. The skin condition is clinically characterized by intense pruritus, relapsing eczematous lesions, and a fluctuating course (Eyerich et al., 2015; Geoghegan et al., 2018), whose manifestations not only have a substantial effect on quality of life by sleep deprivation and profoundly diminished self-esteem (Simpson et al., 2016; Weidinger et al., 2018) but also increase the risk of infection and other atopic disorders (Thaçi et al., 2016). Human commensals producing a novel antibiotic impair pathogen colonization. Our findings demonstrate that human skin … doi: 10.1038/d41586-018-07432-8, Song, W., Anselmo, A. C., and Huang, L. (2019). A. Claesen et al. doi: 10.1016/j.it.2019.08.006, Thaçi, D., Simpson, E. L., Beck, L. A., Bieber, T., Blauvelt, A., Papp, K., et al. Host-microbiome interactions and recent progress into understanding the biology of acne vulgaris. doi: 10.1056/NEJMoa1610020, Sohn, E. (2018). doi: 10.1016/j.jid.2016.01.005, Kasimatis, G., Fitz-Gibbon, S., Tomida, S., Wong, M., and Li, H. (2013). Microbiol. Impact Factor 4.123 | CiteScore 5.4More on impact ›, University of Pennsylvania, United States. A., and Kong, H. H. (2012). Methicillin-resistant Staphylococcus aureus in children with atopic dermatitis from 1999 to 2014: a longitudinal study. After sequential applications of probiotic solutions containing different combinations from one strain to multiple strains of C. acnes on 18 subjects in the first 3 days, the observation demonstrated that the level of engraftment was positively correlated with the presence of several different strains in the probiotic solution, implicating that different strain combinations have synergistic effects on colonization of recipient skin surface and modulation of the C. acnes population at the strain level is feasible by microbiome transplantation. doi: 10.1126/science.aat4326, Summerfield, A., Meurens, F., and Ricklin, M. E. (2015). Sci. Microbiol. doi: 10.1073/pnas.1523199113, Brouns, S. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J., Snijders, A. P., et al. A recent comprehensive review proposes a new concept that AV may be a naturally developing, transient inflammatory interplay of adolescent facial skin with its new microbiota (C. acnes), replacing a state of previous skin homeostasis in childhood (Szegedi et al., 2019). Invest. (2016). Dermatol. What is the human microbiome?. Science 324, 1190–1192. doi: 10.1016/j.anaerobe.2017.04.006, Margolis, J. S., Abuabara, K., Bilker, W., Hoffstad, O., and Margolis, D. J. N. Engl. Dis. J. First-in-human topical microbiome transplantation with Roseomonas mucosa for atopic dermatitis. Composition of the human skin microbiota. Four most prominent bacterial taxa (Actinobacteria, Firmicutes, Bacteroidetes, and Proteobacteria) and the Staphylococcaceae (a Firmicute) are found on the surface of healthy skin. (2019). Our bodies share a symbiotic relationship with trillions of microbes including bacteria, fungi, mites, and viruses.Together, they make up the microbiome, which resides in particular areas of the body such as the skin and gut .. (2017). Furthermore, it is not clear how microbiome transplantation shapes microbial communities on diseased skin via cell-to-cell communication, but the complexity of communication from intraspecies to interkingdom dense network does play an important role in maintaining homeostasis of the cutaneous ecosystem. 8, 2195–2205. Many less severe, but negatively perceived cosmetic skin phenomena are linked with skin microbes, too. Identification of a streptolysin S-associated gene cluster and its role in the pathogenesis of Streptococcus iniae disease. Med. Copyright © 2020 Zhou, Shi, Ren, Tan, Liu and Liu. Recently, Paharik et al. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. In contrast to transplantation of a single microbiota, reintroduction of a cocktail of microbiota has a greater advantage in the level of engraftment. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Skin microbiota analysis. 2020 Sep;34(9):e23363. However, the diversity and relative abundance of the body's microbial communities vary in both the individual and the physiology of the skin sites, which has been categorized into four major skin microenvironment: oily, moist, dry, and foot (Figure 1; Belkaid and Segre, 2014; Byrd et al., 2018). Prevalence and odds of Staphylococcus aureuscarriage in atopic dermatitis: a systematic review and meta-analysis. The skin microbiome is the genetic material of all these microbes. Eur. Although its mechanism is not well-understood, there are already some applications for ecology-based therapy with the aim of correcting the imbalances on the cutaneous ecosystem. This work was supported by the National Natural Science Foundation of China (31470968). The principal intention was to provide an overview of present and future concepts to use skin models in microbiota analyses. Sci. doi: 10.1038/ng.3424, Quan, C., Chen, X. Y., Li, X., Xue, F., Chen, L. H., Liu, N., et al. Under the control of the agr quorum sensing system, the human CoNS species produced AIP to suppress the expression of S. aureus PSMα to prevent S. aureus-mediated epithelial damage and inflammation. Sci Transl. Microbial biofilms are a well-characterized mode of surface-associated growth, which present community-like behaviors. The skin microbiota is indispensable for host skin health, as dermatological conditions have been linked to the alteration of the cutaneous microbiota [ … doi: 10.1186/gm378, Oh, J., Freeman, A. F., Program, N. C. S., Park, M., Sokolic, R., Candotti, F., et al. Human skin microbiota has been described as a "microbial fingerprint" due to observed differences between individuals. There are 1,000 different bacterial species and up to 80 different fungi species. There is no doubt that the composition of the skin microbiota can shift dramatically during the disease progression (Kong et al., 2012). Malassezia leverages the lipids of sebum and the stratum corneum to generate their own lipids in the carbohydrate-deficient and lipid-rich skin setting (Scharschmidt and Fischbach, 2013), which concurs with an enrichment of lipase genes and a depletion of carbohydrate-utilizing enzyme genes in Malassezia spp. Dermatol. As we learn more about how commensal microbiota shape the cutaneous ecosystem, we may be able to leverage this specificity by the reintroduction of living microbiota to govern the skin homeostasis. Genet. Bacteria. There are 1,000 different bacterial species and up to 80 different fungi species. Nat. Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class Mammalia Ashley A. Ross a, Kirsten M. Müller , J. Scott Weeseb, and Josh D. Neufelda,1 aDepartment of Biology, University of Waterloo, Waterloo, N2L 3G1 ON, Canada; and bDepartment of Pathobiology, University of Guelph, Guelph, N1G Human skin is the largest epithelial surface for interaction with microbes. Trends Microbiol. Roseomonas mucosa is one particular commensal found on the skin of healthy and AD individuals (Paller et al., 2019). Here, 3D models offer an unparalleled opportunity to study the human skin microbiota in a functional way. A microbiome-based index for assessing skin health and treatment effects for atopic dermatitis in children. A single application of S. epidermidis strain producing 6-HAP to mouse impaired the incidence of ultraviolet-induced skin tumors. The skin microflora are microorganisms that are resident on our skin. The recently launched Human Microbiome Project aims to characterize the human microbiota and its role in health and disease . 9:eaah4680. The skin is a dynamic and steady ecology that is populated with millions of microbes, such as bacteria, fungi, and viruses, which were collectively termed the skin microbiota (Figure 1; Grice and Segre, 2011). Allergy 68, 498–506. 46, 112–119. doi: 10.1056/NEJMcp033487, Janek, D., Zipperer, A., Kulik, A., Krismer, B., and Peschel, A. The skin’s relatively dry environment and normal microbiota discourage colonization by transient microbes. Cutibacterium and Corynebacterium limited to bacteria, RT6 was found to be enriched in 99 of. 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