Skin microbiome modulation induced by probiotic solutions

Abstract

Background The skin is colonized by a large number of microorganisms, most of which are beneficial or harmless. However, disease states of skin have specific microbiome compositions that are different from those of healthy skin. Gut microbiome modulation through fecal transplant has been proven as a valid therapeutic strategy in diseases such as Clostridium difficile infections. Therefore, techniques to modulate the skin microbiome composition may become an interesting therapeutic option in diseases affecting the skin such as psoriasis or acne vulgaris. Methods Here, we have used mixtures of different skin microbiome components to alter the composition of recipient skin microbiomes. Results We show that after sequential applications of a donor microbiome, the recipient microbiome becomes more similar to the donor. After intervention, an initial week-long phase is characterized by the dominance of donor strains. The level of engraftment depends on the composition of the recipient and donor microbiomes, and the applied bacterial load. We observed higher engraftment using a multi-strain donor solution with recipient skin rich in Cutibacterium acnes subtype H1 and Leifsonia . Conclusions We have demonstrated the use of living bacteria to modulate skin microbiome composition. Electronic supplementary material The online version of this article (10.1186/s40168-019-0709-3) contains supplementary material, which is available to authorized users.

Applications of Human Skin Microbiota in the Cutaneous Disorders for Ecology-Based Therapy

“…Disturbances of the skin microbiota have been directly correlated with multiple diseases. As a result, the novel concept of restoring the composition and functionality of the skin microbiota to the previous indigenous state by targeted manipulation of the skin microbiota, on the basis of the skin ecosystem, has been proposed as a potential therapeutic approach in the last few years (Paetzold et al, 2019;Stacy and Belkaid, 2019). As initial studies of microbiota focused on the gut, which has the largest microbial community in the human body, FMT, a synthetic reproduction of the complex gut ecosystem remaining as most effective therapeutic option with remarkable safety performance, has been applied into clinical practice although not approved by the US Food and Drug Administration (FDA) for clinical use (Cammarota et al, 2017;Allegretti et al, 2019).…”

“…At present, reintroduction of living microbiota (a single or cocktail of microbiota) to modulate skin microbiota composition from disease microbiota states to healthy ones may represent a valid target for ecology-based therapy (Stacy and Belkaid, 2019). 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(Nakatsuji et al, , 2018Williams et al, 2019); (ii) reintroduction of living microbiota induces keratinocytes and sebocytes to produce AMPs to shape microbial communities (Nagy et al, 2005(Nagy et al, , 2006Naik 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). 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.…”

“…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. Paetzold et al (2019) prepared probiotic solutions that were mixtures of different skin microbiome components taken from a healthy donor to modulate the subpopulation of skin microbiota on sebaceous-gland-rich skin regions. 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.…”

“…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. 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). However, the correlation of multidirectional signals in the ecology of skin microbiota is poorly understood.…”

Skin microbiota analysis in human 3D skin models—“Free your mice”

“…[45] Interestingly, there are first promising data available indicating that the microbiota of a recipient becomes more similar to the microbiota of a healthy donor. [46] In this regard, it would be helpful to preselect specific microbiota compo-…”