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Microbiome dynamics of human epidermis following skin barrier disruption
Recent advances in sequencing technologies have enabled metagenomic analyses of many human body sites. Several studies have catalogued the composition of bacterial communities of the surface of human skin, mostly under static conditions in healthy volunteers. Skin injury will disturb the cutaneous homeostasis of the host tissue and its commensal microbiota, but the dynamics of this process have not been studied before. Here we analyzed the microbiota of the surface layer and the deeper layers of the stratum corneum of normal skin, and we investigated the dynamics of recolonization of skin microbiota following skin barrier disruption by tape stripping as a model of superficial injury.
We observed gender differences in microbiota composition and showed that bacteria are not uniformly distributed in the stratum corneum. Phylogenetic distance analysis was employed to follow microbiota development during recolonization of injured skin.
Surprisingly, the developing neo-microbiome at day 14 was more similar to that of the deeper stratum corneum layers than to the initial surface microbiome.
In addition, we also observed variation in the host response towards superficial injury as assessed by the induction of antimicrobial protein expression in epidermal keratinocytes. We suggest that the microbiome of the deeper layers, rather than that of the superficial skin layer, may be regarded as the host indigenous microbiome. Characterization of the skin microbiome under dynamic conditions, and the ensuing response of the microbial community and host tissue, will shed further light on the complex interaction between resident bacteria and epidermis.
The microbial diversity of human microbiota is determined by various factors, such as transmission of non-resident microbes, genetic predisposition, host demographic characteristics, lifestyle and environmental characteristics [ 1 , 2 ].
Humans have a complex interaction with resident microbes as they help us to digest food, and keep us healthy by competing with pathogens and educating our immune system [ 3 , 4 ]. The US National Institute of Health-funded Human Microbiome Project Consortium started 5 years ago to characterize the human microbial communities present at specific body sites, including skin [ 5 , 6 ]. These efforts have recently resulted in an extensive map of the microbes that live in and on us [ 7 , 8 ].
Aberrant microbial compositions have been linked to inflammation-associated human diseases, including specific skin diseases like psoriasis, atopic dermatitis, acne, and chronic skin ulcers [ 9 ]. Skin injury occurs frequently and is likely to have an impact on the skin microbiota.
As skin is relatively easily accessible, and invasive procedures to study skin injury in human subjects are available [ 10 , 11 ], we here studied the dynamics of the cutaneous microbiome in a model for standardized skin barrier disruption. Recently, advanced molecular analyses of skin microbiota have revealed a considerably greater diversity of organisms than presumed from culture-based methods [ 12 , 13 ]. These studies, using either conventional clone sequencing or next-generation sequencing techniques [ 14 ], reported that bacterial diversity mainly depends on the topographical location on the body, and that the observed minimal temporal variability of the skin microbiome appeared to be dependent on the site sampled [ 15 - 19 ].
In general, it was demonstrated that our skin microbiome has a high degree of interpersonal variation with a site-specific composition, but the intra-individual variability of the skin microbiota was reported to be lower when sites with bilateral symmetry were compared [ 15 , 17 , 18 ].
These large scale studies of the composition of microbial communities in healthy volunteers have revealed that most of the resident skin bacteria are categorized into four different phyla: Actinobacteria most dominant reported genera: Propionibacterium and Corynebacterium , Firmicutes majorly represented by Staphylococcus spp.
In addition to its effect on the host, human skin microflora controls colonization by potentially pathogenic microorganisms [ 20 - 23 ], emphasizing the importance of the human skin microbiome in health and disease [ 24 ].
Many human microbiome studies have documented the normal human microbiota composition in a variety of niches and tissues, such as gut, oral cavity, vagina and skin to create a catalogue of resident bacteria using cultivation-independent methods [ 15 , 18 , 25 - 28 ]. In addition, disease state or microbiome recovery following antibiotics therapy have been studied to obtain insight into dynamic and pathological situations [ 29 - 34 ].
Sequencing-based microbiome studies of diseased skin are currently limited to psoriasis [ 35 ], atopic dermatitis [ 36 ], acne vulgaris [ 37 ] and chronic diabetic wounds [ 38 ]. Using conventional clone sequencing, it was found that the bacterial diversity observed in lesional psoriatic skin was greater than for skin from healthy individuals or non-lesional skin from psoriatic patients.
The most abundant and diverse phylum populating the psoriatic lesions was Firmicutes, whereas the phylum Actinobacteria was significantly underrepresented compared to non-lesional skin samples from both healthy persons and patients with psoriasis [ 35 ]. It is, however, unclear if disease-associated changes in the microbiota composition have a causal role or are merely the result of abnormal skin biology observed in inflammatory skin diseases like psoriasis and atopic dermatitis [ 39 ].
In cases where metagenomic studies of the skin microbiome identify groups of microorganisms that are causative, or at least involved in the pathogenesis of diseases, then these will be potential targets for novel therapies. In the present study we investigated whether skin barrier disturbance or skin barrier repair responses affect the host microbiome.
Furthermore, we investigated how microbiota composition differed between layers of the stratum corneum and how these relate to recolonization patterns observed after its removal by tape stripping.
To this end, we have used barcoded pyrosequencing of the V3-V4 region of the 16S rRNA gene for in-depth analysis of microbiota composition of all samples. This study reveals that bacteria are not uniformly distributed in the stratum corneum.
Clear gender differences were identified in upper buttock skin microbiota composition and in the extent of microbiota disturbances after tape stripping. Furthermore, we identified a consistent pattern in microbial community shifts after injury. Our data suggest that the microbiome of the deeper layer of the stratum corneum has an important role in the recolonization process of injured skin. The upper buttock is a standard location for invasive procedures to study skin injury in human subjects [ 11 ].
As this body site was not included in previous microbiome studies [ 18 ], we first analyzed its microbiome composition for comparison with other known locations. We obtained samples from five healthy volunteers in order to analyze the microbial composition of the upper buttock skin, the forehead sebaceous environment and from two moist environments of the body armpit and inner elbow. Notably, the samples of the inner elbow did not cluster together and appeared divided over the three groups. We found that the upper buttock had the largest bacterial diversity of the analyzed sites: In the moist region of the armpit we identified a high proportion of reads assigned to the Firmicutes phylum At other locations of the skin the relative abundances of the phyla Firmicutes and Actinobacteria were differently distributed respectively Furthermore, the higher microbial diversity on upper buttock skin was reflected by the detection of other, relatively low abundant phyla, such as Proteobacteria Clustering, microbial community composition and microbial diversity of samples from different sampling sites.
Composition is displayed as relative abundance, that is, the number of reads assigned to a genus divided by the total number of reads assigned up to the genus level. Participating volunteers are numbered HV1 to HV5 followed by the sampled body location. Colored bars represent the relative abundance of bacterial genera as determined by barcoded pyrosequencing details in Materials and methods. To investigate the composition of microbial communities in different stratum corneum layers we sampled the skin of 12 healthy volunteers at different depths following repeated tape stripping as a method of mechanical removal of stratum corneum layers for detailed description see Materials and methods and Additional file 3.
Samples for microbiome analysis were subsequently taken by swabbing normal skin and the deeper layers of the stratum corneum as exposed by tape stripping. In total, , bacterial 16S rRNA sequences were analyzed, resulting in an average of 5, range 2, to 12, reads per sample Additional file 4.
Redundant analysis also indicated important differences in microbial composition between the superficial and the deeper layer of the stratum corneum blue arrows.
Redundancy analysis of the microbiota composition of the lower back of 12 adults for determining the most important variables 17 in total explaining the variation in microbiota composition at the genus level. Genera that represented at least The first component and second component explain This figure was generated with Canoco version 4. The different variables are represented by arrows, where length reflects significance.
Colors indicate sample groupings: The microbial genera are shown in black text color. UniFrac analysis showed no distinct clustering caused by either tape stripping or gender variables. However, even though the signal is small compared to the differences between volunteers, a small, but potential biologically relevant, signal could easily be obscured by the noise introduced by the individual nature of the samples.
Males have relatively high proportions of Streptococcus, Eremococcus, Finegoldia, Anaerococcus, Veillonella, Sporacetigenium, Corynebacterium, Dermabacter, Brachybacterium, Microbacterium, Dermacoccus and Capnocytophaga when compared to females. Furthermore, females have relatively high proportions of Lactobacillus, Propionibacterium, Gardnerella and Enhydrobacter.
There is also a tendency for higher ratios of Staphylococcus, Janibacter and Brevibacterium in females. Most interestingly, we identified enrichment of Lactobacillus and Gardnerella to be specific for females and Corynebacterium in males.
In addition, one of the Lactobacillus operational taxonomic units OTUs associated with females P -value 0. In the deeper layers of the stratum corneum STR5 and STR10 we found a relative increase in the proportion of the following genera: Furthermore, a relative decrease of Granulicatella, Propionibacterium and Sporacetigenium was found in these deeper layers. Clustering and microbial community composition of different volunteers and epidermal layers.
The figure was generated with iTOL [ 70 ]. Colored bars represent the relative abundance the number of reads assigned to a genus divided by the total number of reads assigned up to the phylum level of bacterial genera as determined by barcoded pyrosequencing. Difference in microbial community composition between males and females. Nodes represent taxa, edges link the different taxonomic levels. The significance is expressed as the P -value of a Mann-Whitney U test of the male and female samples.
Note that the relation between node-size and total abundance is non-linear. Note that the relation between node size and total abundance is non-linear. We investigated the temporal changes in the microbiome composition of the skin surface following mechanical removal of the stratum corneum by tape stripping. Again, the host seems to be the most important denominator of microbiota composition as most of the samples were grouped by individual using hierarchical UniFrac clustering Additional file 5.
It has to be noted that tape-stripped skin at day 14 in general has fully recovered from the initial injury as assessed by clinical not shown and microscopic criteria Additional file 6. Even if the samples from different volunteers differ widely in their constituent taxa, the behavior and dynamics in time can be similar. No difference between partial or complete removal of the stratum corneum was found with respect to microbiome changes in the process of recolonization.
This is illustrated by the pie charts, which respectively correspond to 15 times tape-stripped skin F1 to F3 and M1 to M3 and skin with a completely removed stratum corneum F4 to F6 and M4 to M6. Gender differences also appeared in the recolonization process during the first days after tape stripping, as we observed a relative increase of Propionibacterium , which was a more dominant bacterial group in women, at the cost of Staphylococcus, Corynebacterium and Micrococcus.
The microbiome shifts in response to skin injury were less dramatic in males than in females Additional file 7. The tree-like structure in the left side of the figure is the consensus tree. The pie charts show the microbial community composition of the individual samples. As reported above and described in earlier studies, the microbiota composition varies considerably between individuals [ 15 , 17 , 18 ]. The factors that determine the skin microbiome composition are not known, but host factors involved in innate immunity of the skin are likely to play a role in shaping the microbiome under steady state conditions and following disturbance of homeostasis for example, by skin injury.
Previous work from our lab has shown that expression of antimicrobial proteins is strongly induced following skin barrier disruption [ 11 , 40 , 41 ]. In this part of the study we compared the responses of five healthy controls with respect to induction of eight different antimicrobial proteins.
Note that these individuals were distinct from the volunteers in the tape stripping study from whom no biopsy material was available. Gene expression profiles at baseline and 24 hours after tape stripping of the upper buttock skin were analyzed by quantitative PCR qPCR. Upon tape stripping, all genes showed upregulation, with the highest fold-increases for elafin, MRP8 and psoriasin.
Although the eight genes showed induction in all individuals studied, we observed a hitherto unrecognized large variation between individuals. For example, in individual 1 there was abundant induction of all antimicrobial protein genes except for elafin, whereas individual 3 showed low responses for hBD-3, SLPI, MRP8, psoriasin, LL37, and lysozyme compared to the other individuals while the expression levels of hBD-2 and elafin are the highest in this person.
Variation in the antimicrobial protein host response upon superficial skin injury. Bacterial colonization of human skin starts during birth and continues throughout the first years of life.
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