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Published in final edited form as: Exp Dermatol. 2019 Jan 14;28(2):136–141. doi: 10.1111/exd.13854

Ultraviolet radiation, both UVA and UVB, influences the composition of the skin microbiome

Erin M Burns 1,#, Hana Ahmed 1,2,#, Prescilia N Isedeh 3, Indermeet Kohli 3, William Van Der Pol 4, Abdullah Shaheen 1, Anum F Muzaffar 1, Camli Al-Sadek 1, Thompson M Foy 1, Mohammad S Abdelgawwad 1, Sumeira Huda 1, Henry W Lim 3, Iltefat Hamzavi 3, Casey D Morrow 5, Craig A Elmets 1, Nabiha Yusuf 1
PMCID: PMC7394481  NIHMSID: NIHMS1611748  PMID: 30506967

Abstract

Importance:

Studies have begun to investigate the complex relationship between host and microorganism in non-infectious pathologies such as acne, atopic dermatitis, and psoriasis. Though the skin is continuously exposed to environmental stressors such as ultraviolet radiation (UVR), no studies exist examining the effects of UVR on the skin microbiome.

Objective:

To test the effect of UVA and UVB on human skin microbiome.

Design:

This study was a pilot observational study completed in 2015 and data was analyzed in 2016.

Setting:

The study was conducted in a multicenter setting, utilizing the Henry Ford Hospital and UAB facilities.

Participants:

At the Henry Ford Hospital, individuals with Fitzpatrick types I and II were recruited and consented to the study. Participants were all men (n=6) age 19-35 with no skin disease, photosensitivity, use of photosensitizing medications, antibiotics, or NSAIDs. Participants with tanning bed exposure in the last 6 months were also excluded, and topical medications were not allowed at the site of UVR.

Exposure(s) (for observational studies):

Varying doses of UVA1 and UVB were administered at the Henry Ford Hospital to the skin of the left upper back or midback. The individual minimal erythema dose was determined for both UVA1 and UVB. Control swab samples were taken from non-irradiated skin on the midback. Swab samples were collected prior to, immediately after, and 24 hours after UVR exposure. The swabs were frozen and shipped to UAB. Amplification was done on the V4 region of the 16S rDNA and sequencing was performed at UAB. Various statistical analyses were then conducted on the data to study the population changes.

Main Outcome(s) and Measure(s):

The primary study outcome measurements were statistical changes in the microorganism population as determined by the operational taxonomic unit (OTU) abundance.

Results:

There was vast intra- and inter-subject variation immediately and 24 hours following UVR. Specific observation include an increase in the phylum Cyanobacteria and a decrease in the families Lactobacillaceae and Pseudomonadaceae. The responsiveness of microbes to UVR and their re-colonization potential following exposure differed in UVA vs. UVB.

Conclusions and Relevance:

The results demonstrate that UVR has profound qualitative and quantitative influences on the composition of the skin microbiome, possibly influencing cutaneous disease in which UVR is a factor.

Introduction

The skin is the major interface between an individual and the environment.1 The skin serves several different functions, such as temperature control, water and electrolyte regulation, vitamin D acquisition, and overall, serves as a protective barrier with immune modulation. The skin is also home to prokaryotic microorganisms that in most situations have commensal relationships with the host. The skin can be viewed as an ecosystem, composed of living biological and physical components occupying diverse habitats. In general, the skin is cool, acidic, and desiccated, but distinct habitats are determined by skin thickness, folds, and the density of hair follicles and adnexal structures.2 The physical and chemical features of the skin select for unique sets of microorganisms that are adapted to the niche they inhabit, forming a microbiome.

Furthermore, the cutaneous microbiome has been linked to influencing disease and immunity. Sanford and Gallo demonstrated that in atopic dermatitis flares were associated with a decrease in microbial diversity and an increase in the composition of Staphylococcus aureus.3 The skin microbiome may also play a role in the immune system. One of the methods that commensal microorganisms utilize in immune regulation is inhibiting growth of pathogenic microbes. This can occur by competing for resources (nutrients and space) or through the production of antimicrobial compounds. Commensals have also been found to keep the immune system balanced by preventing over-activity through promotion of immune regulatory cytokines. Lack of exposure to commensals or a change in composition of the microbiome can lead to the production of inflammatory cytokines rather than the immune regulatory cytokines. Chronic inflammation is related to a host of skin diseases.4

As its own ecosystem, human skin and its microbial inhabitants are also subject to the effects of external and environmental stressors, such as ultraviolet radiation (UVR). Environmental factors specific to the individual may modulate colonization of skin microbiota, and knowledge of how they do so can advance our understanding of the delicate balance between host and microorganisms. The effect of external agents on the gut microbiota has been examined using molecular methods,5-7 but an assessment of how environmental agents, such as UVR, affect the skin microbiota in healthy individuals does not exist. Some forms of UVR have well documented bactericidal effects,8 and one can imagine geographical variability in skin microbiota correlating with the longitudinal and/or latitudinal variation in UV exposure. In general, intrapersonal variation in microbial community membership and structure between symmetric skin sites is less than the interpersonal variation, as determined by 16S rRNA metagenomic sequencing.9-11 The purpose of this study was to describe the effects of UVR on the composition of skin microbiome in Fitzpatrick types 1 and 2. We hypothesize that the cutaneous microbiome will change following exposure to UVR and that there will be a difference in the type of change depending on whether it is UVA or UVB light.

Results

UV exposure alters the skin microbiome

Overall, the composition of the microbiome following UVA and UVB radiation was altered, supporting our hypothesis. The alteration in microbiome composition occurred following each UVA or UVB dose, and not a single sample returned to the original pre-UVR composition, regardless of sampling time point (immediately or 24 hours post-UVR). The extent of this change varied widely between individuals. However, some general trends in the samples were observed. One noteworthy phylum level trend was the general increase in Cyanobacteria following UVR exposure; however, it decreased following UVB exposure in one dose in one patient (Fig 1 E-H and Fig 2). Two other phylum trends noted were the increases of both Fusobacteria and Verrucomicrobia following UVR (Fig 1). The family level analysis revealed more consistent trends than the phylum level analysis. Lactobacillaceae decreased following all UVR exposure (Fig 3 and 4). Oxalobacteraceae increased following UVR. Pseudomonadaceae decreased immediately following UVR exposure and decreased to a greater extent following UVA exposure compared with UVB exposure (Fig 4). Overall, Pseudomonadaceae decreased following all UVR exposure from the pre-UVR amount of 3.9%. Pseudomonadaceae only increased in two instances with UVA in this sample, immediately after 27 and 39 J/cm2. This family also increased 24 hours after 250 J/cm2 UVB exposure (Fig 4).

Figure 1. The microorganism composition at the phyla level in male skin varied with UVR exposure.

Figure 1.

Figure 1.

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(A) Immediately following UVA exposure in participant ASC105 and (B) Immediately following UVB exposure in participant ASC105. (C) The microorganism composition at the phyla level in participant ASC105 24 hours following UVA exposure and (D) 24 hours following UVB exposure. (E) The microorganism composition at the phyla level in participant RHM103 immediately following UVA exposure and (F) immediately following UVB exposure. (G) The microorganism composition at the phyla level in participant RHM103 24 hours following UVA exposure and (H) 24 hours following UVB exposure.

Figure 2. The composition of phyla Cyanobacteria increased after UVR exposure in male skin.

Figure 2.

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This increase occurred immediately and 24 hours following (A) UVA exposure in participant ASC105 and (B) UVB exposure in participant ASC105. (C) The composition of Cyanobacteria phyla increased in participant RMH103 with UVB exposure.

Figure 3. The composition of family Lactobacillaceae decreased in participant ASC105 with UVR exposure.

Figure 3.

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This decrease occurred immediately and 24 hours following (A) UVA exposure and (B) UVB exposure.

Figure 4. The microorganism composition at the family level was altered in participant ASC105 following UVR.

Figure 4.

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Microorganism composition depicted immediately following (A) UVA exposure and (B) UVB exposure. Microorganism composition depicted 24 hours following (C) UVA exposure and (D) UVB exposure.

Microbial species diversity in non-irradiated skin

Alpha diversity was analyzed in the pre-UVR samples. Alpha diversity gives insight into the diversity within a species. Observed species and Shannon index were considered. Observed species gives a count of how many total species were available in a sample. Shannon index takes into account richness and evenness, which is the number of different species and the contribution of each composition of species to the overall population. The higher the Shannon index, the higher the richness and evenness, and thus, the higher the diversity. When looking at pre-UVR samples AAP114 and ASC105 (Fig 5) had the highest diversity.

Figure 5. Alpha diversity of pre-irradiated samples of skin.

Figure 5.

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(A) The observed species per sample and (B) the Shannon index of diversity.

Discussion

The biological effects of UVA are usually attributed to increased production of reactive oxygen species, which result in oxidative damage to lipids, proteins, and DNA. On the other hand, UVB photons cause direct damage to DNA, inducing the formation of DNA lesions (photoproducts) such as pyrimidine dimers. These photoproducts block DNA replication and RNA transcription. Exposure to UVB also causes oxidative stress, as demonstrated by the expression of antioxidant defenses following UVB irradiation.18 How microorganisms react and cope with UVR can vary greatly. It has been suggested that Gram-positive bacteria are better adapted to UV stress because their cell walls screen out a significant portion of UVR.19 The results of the current study may be attributed to various unique coping mechanisms inherent in these bacteria.

At the phylum level, one noted trend was the general increase in the composition of Cyanobacteria with UV exposure. While one sample showed a decrease in UVB exposure there was an overall increase in this phylum in comparison with the pre-irradiation samples. Cyanobacteria are Gram-negative bacteria that utilize photosynthesis for energy and produce oxygen. They can produce cyanotoxins, which have been linked to gastrointestinal and hay fever symptoms and pruritic skin rashes. They can also produce lipopolysaccharide, which can irritate the skin.20

Cyanobacteria are believed to have originated in an era in which the ozone was absent, thus it is presumed they faced a high level of UV exposure, which may have shaped their evolution.21 Cyanobacteria produce UV-absorbing compounds, including mycosporine-like amino acids and scytonemin. They are also able to overcome oxidative stress (which has been shown to occur following UVA exposure) through the synthesis of vitamin C, vitamin E, carotenoids, and reduced glutathione. They also have enzymes to counteract oxidative stress, such as superoxide dismutase, catalase, glutathione peroxidase, ascorbate peroxidase, monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase.

Interestingly, Cyanobacteria have received attention for the unique lipopolysaccharide structure and its effect on Toll-Like receptors (TLRs). TLRs recognize pathogen associated molecular patterns (PAMPS), such as LPS in Gram-negative bacteria, or damage associated molecular patterns (DAMPs). One such DAMP is high-mobility group box-1 protein (HMGB1), which is released in response to cellular damage. HMGB1 over-expression has been seen in human neoplasms such as lung, liver, breast, and notably, melanoma.22 After activation, TLRs signal through myeloid differentiation factor 88 (MyD88, leading to NF-kB activation and promotion of inflammation.23 In particular, TLR4 activation has been shown to upregulate immunosuppressive cytokines while also increasing inflammatory cytokines and chemokines, which has been linked to tumor development, growth, and even metastasis.24

Cyanobacterial LPS has a unique structure compared with Gram-negative LPS. It has been found to prevent the signaling cascade that is associated with TLR activation, which has been linked to inflammation and cancer. Cyanobacterial LPS lacks heptose and 3-deoxy-D-manno-octulosonic acid (commonly present in the core region of Gram-negative LPS) and its lipid A region lacks phosphates and contains odd-chain hydroxylated fatty acids.25 In a study evaluating an LPS-like molecule extracted from the cyanobacterium Oscillatoria Planktothrix FP1 (cyanobacterial product, CyP), it was found that CyP is not stimulatory but is a selective antagonist of bacterial LPS. CyP competes with LPS for binding and inhibits the MyD88 pathway (part of the TLR pathway) as well as LPS-induced gene transcription.26

One notable compound, mycosporine-like amino acid (MAA) is a small, colorless, hydrophilic compound found in various organisms from tropical to polar regions. Some MAAs have been found to have a UV absorption maxima between 310-362 nm, which roughly falls into UVA and UVB spectra; it is worth noting that the current study used UVB at 308 nm. MAAs dissipate absorbed radiation as heat and do not produce reactive oxygen species.21 Production of MAAs and other mentioned synthesized substances found in Cyanobacteria may have aided in Cyanobacteria tolerance and increased growth with increased UV exposure as observed in the current study.

In our study, Lactobacillaceae decreased with UVA and UVB exposure at almost every dose. Lactobacillaceae have been shown to play a beneficial role in maintaining health in the skin. A previous study explored the effects of probiotic administration and early UV-induced skin damage. The authors found that intake of Lactobacillus johnsonii is able to protect against UVR-induced damage and accelerate the recovery of skin immune homeostasis following UVR immunosuppression.27 In another study, the effect of lipoteichoic acid (LTA, a component of the cell wall in gram positive bacteria) was investigated for its anti-inflammatory activity and anti-photoaging effects. UVA exposure elevates MMP-1, MMP-3, and MMP-9, which are related to photoaging and inflammation, in normal human dermal fibroblasts. You et al. specifically examined Lactobacillus sakei lipoteichoic acid (sLTA) and its ability to inhibit MMP-1 and MAPK signaling, concluding that sLTA did indeed inhibit these inflammatory pathways. These results also revealed that sLTA is able to repress excessive inflammation produced by LPS, which is found in Gram-negative bacteria.28 The current study demonstrated that increasing amounts of UVR led to a decrease in the overall composition of Lactobacillaceae.

UVA damage is characterized by reactive oxygen species accumulation. Oppezzo et al. found that Escherichia coli, a facultative aerobe, was able to survive UVA exposure levels that Pseudomonas aeruginosa could not. UVA damage affects the chromophores of the respiratory chain, which can cause a halt in the metabolism of a cell. It is proposed that an obligate aerobe, such as P. aeruginosa, could not survive the inhibition of respiration and that a facultative aerobe could withstand this damage.29 In the current study, the family Pseudomonadaceae was a commonly found microorganism on participants’ skin, exhibiting a general decreasing trend following UVR exposure, which may be explained by the intolerance to oxidative damage due to its dependence on aerobic respiration. In conclusion, treatment with UVA and UVB alters the skin microbiome immediately and 24 hours after exposure, specifically in the increase of phylum Cyanobacteria, and decrease in the families Lactobacillaceae and Pseudomonadaceae. Prior to this study, the effects of environmental factors such as UVR on the skin microbiome have not been demonstrated.

Ideas for Future Study

The joint observations that Cyanobacteria are common microorganisms found on the cutaneous surface, that they withstand UVR, and that they have been implicated in preventing TLR4 activation lead to the potential for new areas of research. Future studies include the topical application of Cyanobacteria (or its extracted chemicals of interest) prior to UV exposure and the effect this has on the skin. Another study involves the topical application of Cyanobacteria and/or bacterial products to sites of infection or inflammation due to Gram-negative bacteria.

Additionally, the potential relationship between the protective and anti-inflammatory role of Lactobacillaceae and its subsequent decrease with exposure to UVR could be further explored.

One regrettable factor of the current study was the small number of participants (n=6). Future endeavors to increase the amount of participants, as well as include females and a wider range of Fitzpatrick skin types would be beneficial to acquiring more generalizable findings.

In summary, the current research demonstrates alterations in the skin microbiome following both UVA and UVB exposure. These findings could add new insight into the treatment of UV-induced cutaneous inflammation and other skin diseases linked to microbiome shifts or UVR exposure. There are several potential future studies which would probe the question of a protective nature of microbial inhabitants of the healthy skin microbiome. This may pave the way for the use of prophylactic probiotics for dermatologic health management.

Methods

Subjects

Prior to the start of this study, IRB approval was obtained at Henry Ford Hospital, Detroit MI, and at UAB. Individuals with Fitzpatrick type I (light, pale white; skin always burns, never tans) or type II (white, fair; usually burns, tans with difficulty) were recruited and consented to the study at Henry Ford Hospital. Participants included men (n = 6) between the ages of 19 and 35 years, with no skin disease, no use of antibiotics during time of study, photosensitivity, photosensitizing medications, or NSAIDs. Participants with tanning bed exposure in the previous 6 months were excluded. Topical medications were not allowed at the site of UV exposure.

UV irradiation and sampling

UVA1 (340-400 nm) and narrowband UVB (308 nm) sources were employed in the Dermatology Department at Henry Ford Hospital. Varying doses of UVA1 (22, 27, 33, 39, and 47 J/cm2) and UVB (100, 150, 200, 250, 300, and 350 J/cm2) were applied to the left upper back (UVA1) or midback (UVB). Both irradiated and nonirradiated samples were collected from midback. The individual minimal erythema dose (MED) was determined for both UVB and UVA1. Control swab samples were taken from the non-irradiated skin. Swab samples were acquired immediately following UV exposure and 24 hours post UV exposure. All swabs were dipped in PBS (with 0.5% Tween 20) before swabbing the skin and samples were stored at −80°C until use.

DNA isolation and microbiome analysis

Swab samples were shipped to UAB on dry ice and stored at −80°C until use. DNA from swabs was isolated using Fecal DNA isolation kits from Zymo Research according to manufacturer’s instructions and stored at −80°C for future analysis. To generate an amplicon library for each sample, PCR with bar coded primers was performed to amplify the V4 region of the 16S rDNA gene.14

NextGen sequencing was performed in the UAB Heflin Genetics Core to sequence the products and the dataset were filtered using FastQC to remove reads that did not meet the preset threshold. Tools in the QIIME pipeline were used to identify and cluster taxa, specifically, the RDP classifier was used.14

Tools such as UniFrac15 were used to assess the overall differences between microbiome populations of different samples by principal coordinates analysis. As needed, other analytical packages such as Mothur16 and Genboree17 were evaluated and utilized to extend the capabilities of our current analytical pipeline to further identify and refine microbiota differences between the samples.

Abundance for the top 10 and 25 OTUs were analyzed at the phylum and family level. Reads above 10,000 were the only OTUs analyzed, as contaminated species would be far less abundant (in the 100’s). Patterns and trends were discerned by compositional changes in abundance. Alpha diversity was also examined in men and compared. Shannon diversity and observed species were the main metrics utilized in this analysis. Bray-Curtis and unweighted UniFrac were the metrics utilized in this analysis.

Statistical analysis

Alpha diversity and taxa abundance differences between groups were evaluated using unpaired T-tests. Differences between groups were evaluated using PERMANOVA (weighted UniFrac distance). P values less than 0.05 were considered to be statistically significant. The p-values were generated via a Kruskal-Wallis test. FDR p-value was the p-value corrected by the Benjamini-Hochberg FDR procedure for multiple comparisons.

Key Points.

Question: What is the effect of ultraviolet radiation on the composition of the cutaneous microbiome in humans?

Findings: In this experimental study that included cutaneous microbiome samples from 6 male adults that were subjected to varying ultraviolet radiation A and B, sequencing data revealed changes in the composition of microorganisms inhabiting the skin immediately and 24 hours post-irradiation.

Meaning: Our data demonstrate that ultraviolet radiation has qualitative and quantitative influences on the composition of the skin microbiome, which may have an implication on cutaneous health maintenance or cutaneous pathology.

Acknowledgements

This work was partially supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases 1R01AR071157-01A1 to NY, and a Pilot & Feasibility Study to CDM from NIH funded UAB Skin Disease Research Center grant P30AR050948. The following are acknowledged for their support of the Microbiome Resource at the University of Alabama at Birmingham: School of Medicine, Comprehensive Cancer Center (P30 CA013148), Center for Clinical Translational Science (UL1TR001417), Microbiome Center and Heflin Center for Genomic Sciences. We acknowledge assistance with bioinformatics analysis by Ranjit Kumar and Travis Ptacek.

Footnotes

Conflicts of Interest: The authors have no conflict of interest to declare. IRB approval status: Reviewed and approved by IRB of Henry Ford Hospital: approval #8386.

Statement for prior presentation: This work was presented as a poster at the Society for Investigative Dermatology meeting (2017) in Portland, OR.

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