Portal de Periódicos da CAPES

Microbial Skin Inhabitants: Friends Forever

2016; Cell Press; Volume: 165; Issue: 4 Linguagem: Inglês

10.1016/j.cell.2016.04.035

1097-4172

Pieter C. Dorrestein, Richard L. Gallo, Rob Knight,

Probiotics and Fermented Foods

To gain insight into the stability of the microbial communities that inhabit our skin, Oh et al., in a tour-de-force effort, map the human skin metagenomes over time. Remarkably, their data indicate that the individual, not the environment, primarily drives the composition of skin microbial communities. To gain insight into the stability of the microbial communities that inhabit our skin, Oh et al., in a tour-de-force effort, map the human skin metagenomes over time. Remarkably, their data indicate that the individual, not the environment, primarily drives the composition of skin microbial communities. Previous efforts, including the Human Microbiome Project, showed that microbes inhabit the skin and that different regions of the skin are colonized with different microbes, even within a person (Bouslimani et al., 2015Bouslimani A. Porto C. Rath C.M. Wang M. Guo Y. Gonzalez A. Berg-Lyon D. Ackermann G. Moeller Christensen G.J. Nakatsuji T. et al.Proc. Natl. Acad. Sci. USA. 2015; 112: E2120-E2129Crossref PubMed Scopus (244) Google Scholar, Costello et al., 2009Costello E.K. Lauber C.L. Hamady M. Fierer N. Gordon J.I. Knight R. Science. 2009; 326: 1694-1697Crossref PubMed Scopus (2183) Google Scholar, Grice et al., 2009Grice E.A. Kong H.H. Conlan S. Deming C.B. Davis J. Young A.C. Bouffard G.G. Blakesley R.W. Murray P.R. Green E.D. et al.NISC Comparative Sequencing ProgramScience. 2009; 324: 1190-1192Crossref PubMed Scopus (1840) Google Scholar, Human Microbiome Project Consortium, 2012Human Microbiome Project ConsortiumNature. 2012; 486: 207-214Crossref PubMed Scopus (6942) Google Scholar). The environment established by each unique area of the skin, driven by the oils, salts, pH, peptides, and water, correlates with the composition of these distinct microbial communities(Bouslimani et al., 2015Bouslimani A. Porto C. Rath C.M. Wang M. Guo Y. Gonzalez A. Berg-Lyon D. Ackermann G. Moeller Christensen G.J. Nakatsuji T. et al.Proc. Natl. Acad. Sci. USA. 2015; 112: E2120-E2129Crossref PubMed Scopus (244) Google Scholar, Grice et al., 2009Grice E.A. Kong H.H. Conlan S. Deming C.B. Davis J. Young A.C. Bouffard G.G. Blakesley R.W. Murray P.R. Green E.D. et al.NISC Comparative Sequencing ProgramScience. 2009; 324: 1190-1192Crossref PubMed Scopus (1840) Google Scholar), which extend surprisingly deep into the skin(Nakatsuji et al., 2013Nakatsuji T. Chiang H.I. Jiang S.B. Nagarajan H. Zengler K. Gallo R.L. Nat. Commun. 2013; 4: 1431Crossref PubMed Scopus (304) Google Scholar). However, little is known about the stability of skin microbial communities(Caporaso et al., 2011Caporaso J.G. Lauber C.L. Costello E.K. Berg-Lyons D. Gonzalez A. Stombaugh J. Knights D. Gajer P. Ravel J. Fierer N. et al.Genome Biol. 2011; 12: R50Crossref PubMed Scopus (726) Google Scholar, Costello et al., 2009Costello E.K. Lauber C.L. Hamady M. Fierer N. Gordon J.I. Knight R. Science. 2009; 326: 1694-1697Crossref PubMed Scopus (2183) Google Scholar, Flores et al., 2014Flores G.E. Caporaso J.G. Henley J.B. Rideout J.R. Domogala D. Chase J. Leff J.W. Vázquez-Baeza Y. Gonzalez A. Knight R. et al.Genome Biol. 2014; 15: 531Crossref PubMed Scopus (257) Google Scholar), and the viral and fungal community stability in the skin is essentially unknown. Building on their previous studies, Oh et al., 2016Oh J. Byrd A.L. Park M. Kong H.H. Segre J.A. NISC Comparative Sequencing ProgramCell. 2016; 165 (this issue): 854-866Abstract Full Text Full Text PDF PubMed Scopus (495) Google Scholar, in this issue of Cell, now use shotgun metagenomic sequencing to provide a comprehensive inventory of the bacteria, fungi, and viruses on human skin, at both short (1–2 months) and long (1–2.5 years) intervals, to evaluate the stability of the microbial communities that inhabit our skin (Figure 1). The metagenomic inventory was accomplished using low-biomass samples, providing data not only into the stability of bacterial taxa, as most previous studies had focused on, but also gaining insight into the overall metabolism of the community through mapping functional genes across all taxa, including the fungal and viral inhabitants. The inventory, of 12 participants, reveals that the community is reflective of the person, but also shows that variability exists and that this is dependent on location on the body (Figure 1). Pioneering descriptive studies such as this metagenomic inventory provide a critical resource for understanding the skin microbiome, open our eyes to how little we know about the temporal stability of the skin microbiome and about our fungal and viral partners, and enable many different hypotheses to be formulated, all of which are now very feasible to test with advances in technology. The long duration of the time series, and the matched samples across multiple sites in the same individuals, allows us to understand which sites on the body are most and which are least stable and the relationship in variability in the different taxa. Fascinatingly, and in contrast to previous work, the individual rather than the environment seems to drive the microbiome overall. The skin environment has remarkably diverse chemical and physiological microenvironments, and it is surprinsing that the individual differences at the strain level can overcome these differences to establish the microbial community. Although there is variation at other sites in the body colonized by bacteria, such as the gut and the mouth, and similar questions about regional stability apply, the skin has an especially high diversity of environments and exposures. Although this work represents a significant advance, there is still much more to be done. The work was performed on a small adult cohort, and we know that pediatric populations differ in their microbiomes across the body (Costello et al., 2013Costello E.K. Carlisle E.M. Bik E.M. Morowitz M.J. Relman D.A. MBio. 2013; 4 (e00782-e13)Crossref Scopus (106) Google Scholar). Whether this variation extends to the variability in the microbiome as well as its current state remains to be seen, and early infancy and puberty may be times where the skin microbiome is particularly perturbed. Similarly, populations with different microbial and lifestyle exposures, including those living very traditional lifestyles in environments ranging from the tropics to the arctic, have different baseline skin microbial populations(Clemente et al., 2015Clemente J.C. Pehrsson E.C. Blaser M.J. Sandhu K. Gao Z. Wang B. Magris M. Hidalgo G. Contreras M. Noya-Alarcon O. et al.Sci Adv. 2015; 1Crossref PubMed Scopus (495) Google Scholar) and may have different dynamics. Skin diseases, such as eczema, transiently change the microbiome, but the influence of other disorders or medications is not well understood. Using metagenomics to read out "functional capacity" does not reveal function per se: linking these studies to metabolomic and immunological readouts will be especially effective for understanding how much functionality changes along with taxonomy. Finally, it is unclear how far the stability goes in terms of its resistance to deliberate manipulation. Given the profound effect that consumer products have on our skin metabolite repertoire (Bouslimani et al., 2015Bouslimani A. Porto C. Rath C.M. Wang M. Guo Y. Gonzalez A. Berg-Lyon D. Ackermann G. Moeller Christensen G.J. Nakatsuji T. et al.Proc. Natl. Acad. Sci. USA. 2015; 112: E2120-E2129Crossref PubMed Scopus (244) Google Scholar), is it possible to alter the skin microbiome either through a single change or through repeated exposure, and what are the implications of these alterations for long-term skin health and perhaps for systemic immune effects? The methods established here for improving yield of fungi and viruses and for handling small samples, as well as the improved baseline insight into the skin microbiome across taxa, is critical for advancing the field in these directions. In particular, the role of the human body as a dynamic system is underappreciated in medicine, and understanding which measurements of skin are more stable or less stable is critical in clinical settings, especially when baselines may need to be established per subject and per body site rather than at the population level. Extending these studies to include other "omics" levels, for which metagenomics is a key underpinning, will help us develop reliable and robust biomarkers for health and disease. There is tremendous potential for applying these techniques to see what goes wrong, not just with the static state of the microbiome but in its dynamics for a range of skin diseases. For example, are there "basins of attraction" where more intrinsically variable microbiomes are more likely to fall into those basins or to escape them? Are there very precise pathways in dynamic space that lead to different diseases? What are the best early warning signs and at which chemical, gene expression, or taxonomic level can they best be read out? Is it possible to design a wearable sensor that gives frequent measurements of a specific chemical or genetic subspace of the full dataset, allowing long-term monitoring and maintenance of skin health? Can microbes be used as "stem cells" to reconstitute essential functions that should be performed by the normal skin microbiome but are deficient due to environmental or host dysfunction? The present work provides a fundamental resource allowing such questions to be asked, and as the costs of the component omics analyses continue to drop, the ability to monitor large, diverse populations under different intervention scenarios will revolutionize our understanding of the skin microbiome and its role in disease and guide personalized interventions. Temporal Stability of the Human Skin MicrobiomeOh et al.CellMay 05, 2016In BriefHealthy adults stably maintain their skin microbial communities over time at the kingdom, phylum, species, and even, strain level, despite constant exposure to the external environment and other individuals. Full-Text PDF Open Archive