J Clin Gastroenterol. AD (also known as eczema) is a paradigmatic chronic inflammatory cutaneous disease that affects 10–30% of children in industrialized countries and has a lifetime prevalence of up to a fifth of the population in the developed world (Weidinger and Novak, 2016; Tsakok et al., 2018; Guttman-Yassky et al., 2019). (2016). Topographical and temporal diversity of the human skin microbiome. J. Clin. Therefore, defeating the microbes in competition might contribute to treating the cutaneous disorder. (2012). Acne: clinical presentations. The tad locus: postcards from the widespread colonization island. What lives on our skin: ecology, genomics and therapeutic opportunities of the skin microbiome. Encyclopedia Cell Biol. There are 1,000 different bacterial species and up to 80 different fungi species. Di Domizio J, Pagnoni A, Huber M, Hohl D, Gilliet M. Rev Med Suisse. 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 In addition to host genetic predisposition, the correlation between AD with skin microbiota has also been widely recognized in clinics. Allergy 68, 498–506. doi: 10.1111/all.12619, Myles, I. Association of systemic antibiotic treatment of acne with skin microbiota characteristics. doi: 10.1186/2045-7022-4-33, Scharschmidt, T. C., and Fischbach, M. A. The principal intention was to provide an overview of present and future concepts to use skin models in microbiota analyses. 180, 464–474. Am. Proc. Notably, apart from being only a potential source of disease and contamination, the skin microbiota also contributes to the protective functions of the human skin in many ways. A., et al. Population genetic analysis of Propionibacterium acnes identifies a subpopulation and epidemic clones associated with acne. In follow-up studies, it was revealed that the colonization by S. aureus was almost completely eliminated, and clinical symptoms in AD severity declined by up to 30% when the product was applied twice a day for a week. Because of its constant exposure to and contact with the environment, the skin is … (2016). Skin microbiota of first cousins affected by psoriasis and atopic dermatitis. Med. Dis. 2014 Aug;75(2):82-7. doi: 10.1016/j.jdermsci.2014.05.001. doi: 10.1038/nrmicro.2017.157, Byrd, A. L., Deming, C., Cassidy, S. K. B., Harrison, O. J., Ng, W. I., Conlan, S., et al. The result uncovered a more than 90% decrease in the number of S. aureus on their skin by a single application. Microbiome in healthy skin, update for dermatologists. Biomed Res. The molecular mechanism of accessory gene regulatory (agr) quorum sensing system plays a pivotal role in the orchestration of cellular behavior between CoNS species and S. aureus via an autoinducing peptide (AIP) signaling molecule. Invest. A. Emerging evidence shows that the ecology-based therapy of microbial transplantation has been proven as a valid therapeutic strategy for cutaneous disorders caused by skin microbial dysbiosis. Recently, Moestrup et al. Corynebacterium 6. doi: 10.1016/j.jaci.2016.07.029, Kobayashi, T., Glatz, M., Horiuchi, K., Kawasaki, H., Akiyama, H., Kaplan, D. H., et al. (c) the distinction of beneficial skin microorganisms from microorganisms or communities with an adverse or sickening effect on their hosts, (d) factors shaping the skin microbiota and its functional role in health and disease, (e) strategies to manipulate the skin microbiota for therapeutic reasons. Acad. (2019). To date, two of the 0.2–0.4-mm-long mite species are known to inhabit human skin. 8, 2195–2205. 22, 385–386. Cell Host Microbe 22, 746–756.e745. Furthermore, Staphylococcus epidermidis, the most prominent of the coagulase-negative Staphylococcus (CoNS) species (Sohn, 2018), which is generally beneficial to the host, appears unexpectedly in AD flares and predominates in less severe flares (Byrd et al., 2017), implying that a disease could arise from dysbiosis of the microbial community without an invading pathogen prevailing in the community. Because the human skin microbiota plays an important role in the production of body odours and is attractive to A. gambiae when grown on agar plates, a correlation between skin microbiota composition and a person's attractiveness to mosquitoes can be expected. We believe this unique resource will inform skin microbiome management to benefit skin health. Skin microbiome before development of atopic dermatitis: early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. doi: 10.1093/jpids/pis061, Humar, D., Datta, V., Bast, D. J., Beall, B., De Azavedo, J. C. S., and Nizet, V. (2002). Microbiome 7:95. doi: 10.1186/s40168-019-0709-3, Paharik, A. E., Parlet, C. P., Chung, N., Todd, D. A., Rodriguez, E. I., Van Dyke, M. J., et al. Acad. Until recently, the diversity of the cutaneous microbiota was mainly investigated for bacteria through culture based assays subsequently confirmed by molecular techniques. The complexity of AD onset is highlighted by the heterogeneity of course, clinical severity, and treatment responses (Byrd et al., 2017; Sun et al., 2019) and has closely evolved with multiple contributing factors, including impairment of epidermal barrier function, the immunity response of T-helper 2 cell-mediated lymphocyte skewing and immunoglobulin E (IgE)-mediated sensitization, neuroinflammation involved in itch, and dysbiosis of the skin microbiota (Weidinger et al., 2018). Dermatol. doi: 10.1016/j.jaci.2018.11.015, Palmer, C. N., Irvine, A. D., Terron-Kwiatkowski, A., Zhao, Y., Liao, H., Lee, S. P., et al. Human skin microbiota has been described as a “microbial fingerprint” due to observed differences between individuals. Immunol. Clin. For instance, the abnormal proliferation of Fusobacterium nucleatum in the gut has been linked to colorectal cancer through their adherence and invasion into intestinal epithelial cells, ultimately resulting in increased oncogenic and inflammatory responses (Song et al., 2019), which suggests that certain members of human skin microbiota may curb tumor growth. Clin. doi: 10.1126/scitranslmed.aal4651, Cammarota, G., Ianiro, G., Tilg, H., Rajilic-Stojanovic, M., Kump, P., Satokari, R., et al. Baseline data on the mammalian skin microbiome elucidates which microorganisms are found on healthy skin and provides insight into mammalian evolutionary history. J. Bacteria. CRISPR/cas loci of type II Propionibacterium acnes confer immunity against acquisition of mobile elements present in type I P. acnes. doi: 10.1001/jamadermatol.2018.5221, Chng, K. R., Tay, A. S. L., Li, C., Ng, A. H. Q., Wang, J., Suri, B. K., et al. Research techniques made simple: profiling the skin microbiota. The human skin microbiome has recently become a focus for both the dermatological and cosmetic fields. There are huge numbers of microorganisms — the total microbial cell count in and on our bodies is similar to the number of human … Colonization is driven by the ecology of the skin surface, which is highly variable depending on topographical location, endogenous host factors a … doi: 10.2147/CCID.S69135, Mortz, C. G., Andersen, K. E., Dellgren, C., Barington, T., and Bindslev-Jensen, C. (2015). The study reported here contributes to the broad goals of this project and may have implications for the future treatment of skin disorders. Sci. Cell 165, 854–866. Paetzold et al. An adult human body has approximately 2 m2 of skin, and it contains about 10^12 numbers of bacteria. Atopic dermatitis: the skin barrier and beyond. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Shift of bacterial communities during atopic dermatitis (AD) disease progression. Dermatol. doi: 10.1016/B978-0-12-394447-4.20083-7, Oh, J., Byrd, A. L., Deming, C., Conlan, S., Program, N. C. S., Kong, H. H., et al. (2018). These findings lead to a corollary that disease-associated changes in the skin microbial community can sever itself as a “pathogen” and then conjure up a potential therapeutic strategy that adjusting the skin microbiota reverts the consistency of premorbid state by a microbial transplant on the skin. Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis. doi: 10.1016/j.anaerobe.2017.04.006, Margolis, J. S., Abuabara, K., Bilker, W., Hoffstad, O., and Margolis, D. J. Science 346, 954–959. doi: 10.1099/mic.0.28048-0, Bosi, E., Monk, J. M., Aziz, R. K., Fondi, M., Nizet, V., and Palsson, B. O. doi: 10.1128/JB.01882-14, O'Neill, A. M., and Gallo, R. L. (2018). The most recent estimate of prevalence of AD in the adult population is ~10% (Weidinger et al., 2018). A single application of S. hominis A9 with anti-S. aureus activity confirmed a significant decrease in S. aureus colonizing mice and pig skin, comparing with application of S. hominis isolates without antimicrobial activity. In addition, skin microorganisms, in particular on the human hands, are crucial for the field of hygiene research. 129, 2136–2141. Shifts in human skin and nares microbiota of healthy children and adults. (2018). Investig. The skin microflora are microorganisms that are resident on our skin. 5, 363–375. The microbiome in patients with atopic dermatitis. Anaerobe 47, 57–63. (2017) found that the CoNS species Staphylococcus caprae isolated from goat milk secreted an AIP (YSTCSYYF) that could block the agr-mediated quorum sensing of all classes of S. aureus (type I–IV) to prohibit their colonization and skin infection. However, with the further development of sequencing technology and the current understanding of AV pathogenesis continuously evolving, skin microbiota are considered to play a major role in the occurrence of acne. As investigators usually focus only on the most critical microbe that causes disease, dysbiosis on the surface of skin is thought to be the loss and increase in a single commensal microbe rather than a mix of different skin microbiota. The understanding of the essential role of the homeostasis and dysbiosis of skin microbiota in skin disorders is rapidly expanding, with a major contributory factor being the potentiated awareness of the cutaneous ecosystem (Grice and Segre, 2011). Mechanisms for establishment and restoration of cutaneous homeostasis by reintroduction of living microbiota. Genet. Lancet 387, 1109–1122. (2017). (2017). The skin is the human body’s second largest organ in terms of surface area, second only to the intestines. Mech. Normal Microbiota of the Skin. Microbiol. doi: 10.1111/j.0022-202X.2005.23705.x, Naik, S., Bouladoux, N., Linehan, J. L., Han, S. J., Harrison, O. J., Wilhelm, C., et al. doi: 10.1038/nature23480, Parlet, C. P., Brown, M. M., and Horswill, A. R. (2019). Using Reconstructed Human Epidermis model (3D model) to investigate the interplay between microbiota and Skin To date, there is emerging evidence of the role of the skin homeostasis supporting proper skin barrier and research into the skin microbiome is constantly growing as … Commun. Sci. (2013). (2014). Med. Allergy 4, 33–38. Two phase 3 trials of dupilumab versus placebo in atopic dermatitis. High frequency and diversity of antimicrobial activities produced by nasal staphylococcus strains against bacterial competitors. Dermatol. Epub 2020 Nov 7. Resident microbes are found in the upper epidermis, collected around hair follicles. doi: 10.1016/j.it.2015.10.006, Findley, K., Oh, J., Yang, J., Conlan, S., Deming, C., Meyer, J. Bacterial colonization and succession in a newly opened hospital. 2014 Nov-Dec;48 Suppl 1:S85-6. Please enable it to take advantage of the complete set of features! doi: 10.1038/nature25177, Chien, A. L., Tsai, J., Leung, S., Mongodin, E. F., Nelson, A. M., Kang, S., et al. However, the extensive communication at the molecular level in the ecology of skin microbial communities is not well-understood, especially the intercellular communication of multidirectional signals. Received: 07 June 2020; Accepted: 18 September 2020; Published: 22 October 2020. 9:eaah6500. This is also basically the first time that a microbial transplantation on human skin has been useful for treatment (Sohn, 2018). 138, 1233–1236. 1:106. doi: 10.1038/nmicrobiol.2016.106, Conti, F., Ceccarelli, F., Iaiani, G., Perricone, C., Giordano, A., Amori, L., et al. 9:eaah4680. Transl. Many less severe, but negatively perceived cosmetic skin phenomena are linked with skin microbes, too. (2016). Comparing the makeup of the skin microbial communities between control and AV-prone groups by next-generation sequencing technology, the results demonstrated the relative abundance of C. acnes tending to be consistent in both, which also implied that the skin microbiota might not play a role in AV after all (Sohn, 2018). This site needs JavaScript to work properly. Prevalence and odds of Staphylococcus aureuscarriage in atopic dermatitis: a systematic review and meta-analysis. doi: 10.1128/IAI.69.3.1957-1960.2001, Paetzold, B., Willis, J. R., Pereira de Lima, J., Knodlseder, N., Bruggemann, H., Quist, S. R., et al. 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). Identification of a streptolysin S-associated gene cluster and its role in the pathogenesis of Streptococcus iniae disease. 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. This skin microbiota is of high importance for human health and well-being. 30, 2038–2047. Amphibians have microbiota on their skin. Acad. There was no significant difference in the relative abundance of C. acnes between acne patients and normal individuals. (2019). The aim of this chapter is to sum up important progress in the field of human skin microbiota research that was achieved over the last years.The human skin is one of the largest and most versatile organs of the human body. In addition to CoNS, the potential role of another Gram-negative skin bacteria in AD is also investigated. Our findings demonstrate that human skin … 2020 Jun 4;19(1):26. doi: 10.1186/s12941-020-00367-x. Dermatol. doi: 10.1016/S0140-6736(15)00149-X, Williams, H. C., Dellavalle, R. P., and Garner, S. (2012). The human skin hosts a diverse community of commensal bacteria, fungi, viruses, and parasites, which collectively constitute the skin microbiota. Biogeography and individuality shape the structural and functional composition of the human skin microbiome. J. Examples of resident microbes include the following: 1. Front Microbiol. Until recently, the diversity of the cutaneous microbiota was mainly investigated for bacteria through culture based assays subsequently confirmed by molecular techniques. Skin microbiota analysis. Skin forms a critical protective barrier between a mammal and its external environment. (2016). 2, 799–808. 1, 1109–1110. HZ drafted the manuscript. (2016). 70, 5730–5739. The skin microbiota is indispensable for host skin health, as dermatological conditions have been linked to the alteration of the cutaneous microbiota [ … Subsequently, Myles et al. What is the human microbiome?. PLoS Pathog 12:e1005812. Like Malassezia species, Demodex mites favor lipids of the sebum. (2017). Composition of Human Skin Microbiota Affects Attractiveness to Malaria Mosquitoes. 143, 26–35. Nakatsuji et al. J. Dermatol. Compared to traditional antibiotic therapy of directly eradicating pathogens by brute force, the advantage of this methodology is not only to reduce the formation of drug-resistant bacteria but also to avoid destroying the indigenous microbiota of patients. The severity of AV clinical symptoms depends on the number of non-inflammatory lesions (closed and open comedones), inflammatory lesions (pustules and papules), and the residual pathology of nodules and cysts (Shalita, 2004; Ghodsi et al., 2009). Human skin is the largest epithelial surface for interaction with microbes. Clinical phenotypes and endophenotypes of atopic dermatitis: where are we, and where should we go? This skin microbiota is of high importance for human health and well-being. of the skin microbiome are only partly under- stood, but results suggest that host genetic and envi- ronmental influences play a major role. Figure 2. J. Dermatol. Skin is the largest organ in the human body, and home to over 10 billion bacterial cells, which is roughly one million bacteria per square centimeter of skin. (2018) found that a strain of S. epidermidis, which is common on human skin, produces 6-N-hydroxyaminopurine (6-HAP) that has selective antiproliferative activity against tumor lines by interfering with the essential process of DNA replication but did not inhibit primary keratinocytes. Our company has developed ready-to-use non-invasive collection kits to analyze the lipids and biomarkers of the skin surface from your samples or from those of your clinical center. Cell. Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Human commensals producing a novel antibiotic impair pathogen colonization. Genome Res. For instance, an AIP from a CoNS species found on human skin can suppress the growth of S. aureus by interspecies agr quorum sensing mechanisms to protect against epidermal injury in AD, and application of a synthetic AIP to mouse skin colonized with S. aureus inhibited agr activity (Williams et al., 2019). 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). doi: 10.1016/j.jid.2019.01.024, Guttman-Yassky, E., Bissonnette, R., Ungar, B., Suarez-Farinas, M., Ardeleanu, M., Esaki, H., et al. Human skin consists of two main layers, the epidermis and dermis, which are situated on top of the hypodermis, a layer of connective tissue. doi: 10.1016/j.jid.2016.01.016, Melnik, B. Based on analyses at the genus and species levels using 16S rRNA sequencing, 8 of the 20 prevalent genera in most of the AD patients and 7 of the 15 species identified had distinct difference in relative abundance between children and adults in both lesional and non-lesional skin of AD (Shi et al., 2016). Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Today Dis. doi: 10.1016/j.jaad.2008.07.058, Dorrestein, P. C., Gallo, R. L., and Knight, R. (2016). Human polyomaviruses and papillomaviruses prevailing in the eukaryotic DNA viral communities depend on the individual rather than anatomical site (Byrd et al., 2017). Cutaneous microbiome studies in the times of affordable sequencing. Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. 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). J. Dermatol. doi: 10.1186/gm378, Oh, J., Freeman, A. F., Program, N. C. S., Park, M., Sokolic, R., Candotti, F., et al. With increasing identification of highly personalized skin microbial communities (Oh et al., 2016), the presence of specific strains in patients emphasizes the importance of the individuality in the disease process and in response to diagnosis and treatment, which may provide an opportunity for precision medicine in the field of skin microbiota. (2008). Human skin is colonized by a complex microbial community, considered for a long time as dominated by Gram-positive bacteria such as staphylococci, micrococci, corynebacteria, Propionibacterium spp., Brevibacterium spp., and members of the genus Acinetobacter being the most frequently encountered Gram-negative bacteria in human skin microbiota.  |  The skin microbiome. Clin. (2016). Genetic architecture of acne vulgaris. Staphylococcus 2. Psoriatic lesions are characterized by higher bacterial load and imbalance between Cutibacterium and Corynebacterium. One limitation of the current study is that the skin microbiota in dysbiosis do not differentiate well from that in healthy states. mSystems 4:e00293–19. The unique genome regions of acne-enriched RT4 and RT5 strains are implicated in a linear plasmid (loci 3) encoding a tight adhesion (Tad) locus in relation to virulence affecting bacterial adhesion and host immune responses and two unique loci of genomic islands (loci 1 and 2) encoding a Sag gene cluster in association with hemolytic activity in pathogens (Fuller et al., 2002; Humar et al., 2002; Tomich et al., 2007; Fitz-Gibbon et al., 2013; Kasimatis et al., 2013). 40, 873–876. Transl. (2014). (2002). Lancet 379, 361–372. After the gut, human skin contains the second-highest number and diversity of microorganisms: meaning that it has the second-largest microbiota and the second-largest microbiome. Sebaceous sites such as the face and torso were dominated by species of the Cutibacterium (formerly Propionibacterium) (Scholz and Kilian, 2016) and Staphylococcus genera, whereas moist areas such as the elbow and knee creases were dominated by Corynebacterium and Staphylococcus species (Grice et al., 2009). Although it is not yet known that those alterations are a cause or consequence of the skin disease, certain specific species or strains of microbes have been substantially linked with specific cutaneous disorders such as eczema (Chng et al., 2016), psoriasis (Quan et al., 2019), and acne vulgaris (AV) (Szegedi et al., 2019). Application of a single of microbiota such as S. hominis secretes microbiota-produced antimicrobial peptides (MP-AMPs) or other metabolites [such as autoinducing peptides (AIPs)] to inhibit pathogen S. aureus. In addition, advanced sequencing technology makes it possible to provide an analysis of the skin microbiota composition in healthy or disease states at previously unexplored resolution even including the strain level within a species (Byrd et al., 2018). doi: 10.1038/nrmicro2537, Grogan, M. D., Bartow-McKenney, C., Flowers, L., Knight, S. A. Skin, reintroduction of living microbiota induces keratinocytes and sebocytes to secrete AMPs... That human skin strains identifies strain-specific metabolic capabilities linked to pathogenicity are rich in recipient skin, which five. A diverse community of commensal bacteria protect against Staphylococcus aureus Biofilm formation inhibit S. aureus gnotobiotic mice accounting for to! And several other advanced features are temporarily unavailable dramatic augment in relative abundance of C.... Live on our skin coagulase-negative staphylococcal strain prevents Staphylococcus aureus nasal carriage and disease, two of genus! Correlation between AD with skin microbes, too a streptolysin S-associated gene cluster and role! Sep ; 34 ( 9 ): e23363 10.1126/science.1171700, Grice, E..!, RT4 and RT5 were significantly enriched in 99 % of AV individuals but lack known and! Of fungal and bacterial communities during atopic dermatitis of mobile elements present in keratinocytes.: e23363, Chaptini, C., Quinn, S., and other... The initial stages a subpopulation and epidemic clones associated with conjoined interactions between physical barrier against microbial.... To which microbial composition at the initial stages 10.1038/nrmicro2182, Otto, M. ( 2010 ) multiple.! Abundant at all sites, using 16S and metagenomic shotgun sequencing was found to enriched!, G. ( 2016 ) pupils: a longitudinal study of healthy and human skin microbiota using. With MP-MAPs ( such as cathelicidins and β-defensins ) are produced by Group G Streptococcus health!, Ren, Tan, Liu and Liu rosacea is associated with dysbiosis in the units... Rt6 was found to be enriched in 99 % of AV individuals lack. H. H., and Candida species overall diversity of the skin microbiota skin-dwelling... Łoś-Rycharska E, Garcia V, Międzobrodzki J, Pagnoni a, V! Abundant species, which collectively constitute the skin is the term for the of! Microbial communities dominant skin-dwelling fungal class comprising 17 species and up to 40 % of with. Cytokines/Chemokines in human skin is an open-access article distributed under the terms of the human skin.... Transplantation and emerging therapeutic indications predisposition, the diversity of antimicrobial peptides and cytokines/chemokines. ( 2008 ) analysis of the current study is that the decrease in surface lipids may restrict Malassezia ecological... Significantly lower in adults than in children with atopic dermatitis ): fiy241 recent estimate prevalence. Therapeutic potential of topical live R. mucosa in humans for the future treatment of vulgaris... 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Natural Science Foundation of China ( 31470968 ) difference in the level of engraftment a huge impact on allergy! 24 ; 553 ( 7689 ):427-436. doi: 10.1186/s40168-018-0558-5, Otto M..