The Dark Side of Sunlight: How it Impacts Your Microbiome

Introduction

The human skin is constantly exposed to various environmental factors, with ultraviolet radiation (UVR) being a major influence on skin health and disease. UVR is divided into UVA, UVB, and UVC. Sunlight primarily consists of UVA (90–95%) and a smaller portion of UVB (5–10%), while UVC is almost entirely absorbed by the ozone layer and does not reach the Earth's surface (Rai, Rai & Kumar, 2022). Both UVB and UVA can lead to DNA damage, oxidative stress, premature aging, and an increased risk of skin cancer. Additionally, UVR has been linked to immune suppression and may significantly affect the skin’s microbiome. Hence, photoprotective measures are important to consider in order to protect the skin against the harmful effects of UVR (Grant, Kohil & Mohammad, 2024).

Is UVR good or bad?

UVR has several positive effects, including the activation of anti-inflammatory and immunosuppressive pathways, which benefit various skin conditions like psoriasis, atopic dermatitis, vitiligo, graft-versus-host disease, and can influence certain infections as UVR promotes vitamin D production, which may help reduce the risk of respiratory tract infections and tuberculosis (TB), with higher solar UVB exposure linked to lower TB incidence. UVR also enhances immune responses, such as macrophage activity and antimicrobial peptide production, which aid in combating infections (Hart et al., 2019). 

Beyond skin diseases, UVR also plays a beneficial role in systemic conditions such as asthma, multiple sclerosis, schizophrenia, type 1 diabetes, autism, and cardiovascular diseases. These effects result from interactions between UVR-induced regulatory cells and mediators like nitric oxide, interleukin-10, and 1,25-dihydroxy vitamin D3 (Rai, Rai & Kumar, 2022). Moderate exposure to UV radiation is also beneficial for health and plays a crucial role in the production of vitamin D (Xiaoyou et al., 2024).

Prolonged UVR exposure can generate reactive oxygen species (ROS) both directly by affecting cellular components and indirectly through photosensitization mechanisms. Indirectly produced ROS include various species such as superoxide anions (O2.-), singlet oxygen, hydroxyl radicals, and hydrogen peroxide, formed through different pathways. These free radicals can be further converted into other ROS types. Low ROS levels can cause mutations, medium levels may induce cellular senescence, and high levels typically lead to cell death, including apoptosis and necrosis (Figure 1) (Xiaoyou et al., 2024).

UVR damages DNA as well through two main mechanisms: direct and indirect. Direct damage, primarily from UVB rays, leads to the formation of cyclobutane pyrimidine dimers (CPDs) and 6-4 photoproducts, which distort the DNA structure. Indirectly, UVA radiation generates reactive oxygen species (ROS) that oxidize DNA bases, causing mutations like 8-oxoguanine  (Figure 1) (Xiaoyou et al., 2024). Both types of damage can impair DNA repair, leading to mutations, skin aging, and an increased risk of skin cancers. 

Figure 1: UVR triggers the production of reactive oxygen species (ROS) and causes DNA damage. Chromophores absorb UV light, generating ROS such as superoxide anions (O2.-), singlet oxygen, hydroxyl radicals, and hydrogen peroxide through various pathways. UV-induced DNA damage primarily results in the formation of cyclobutane-pyrimidine dimers (CPDs) and 6-4 photoproducts (6-4PP), typically at dimerization sites. ROS can also contribute to single-strand breaks (SSBs) and double-strand breaks (DSBs) in DNA. Image taken from (Xiaoyou et al., 2024).

UV radiation (UVR) affects different age groups in distinct ways. Children generally face a lower risk of UV-related skin damage compared to adults. However, certain UV-induced conditions, such as photoaging (early skin wrinkling), freckles, and moles, can manifest during childhood and adolescence. Severe UV damage in early life may also increase the risk of long-term complications, including benign and malignant skin tumors, such as melanoma, basal cell carcinoma (BCC), and squamous cell carcinoma (SCC), later in adulthood (Green, Wallingford & McBride, 2011).

In Japanese populations, the first sign of photoaging typically appears as solar lentigines on the face around the age of 20. This is followed by the development of fine wrinkles after 30, and benign skin tumors, like seborrhoeic keratoses, commonly appearing on sun-exposed skin after 35 (Ichihashi & Ando, 2014). 

The response to UVR also varies with age at the cellular level. Younger skin has more efficient DNA repair mechanisms, while aging skin experiences increased DNA damage and impaired repair capacity due to the presence of senescent fibroblasts and reduced production of insulin-like growth factor-1 (IGF-1) (Kemp, Spandau & Travers, 2017).

While UVR is essential for our health by aiding in vitamin D production and providing therapeutic benefits, excessive exposure poses serious risks. To enjoy the advantages of UVR while reducing its harmful effects, it’s crucial to implement preventive and protective measures. A key aspect of this understanding lies in recognizing the relationship between UV radiation and the skin microbiome.

Skin Microbiome

The human skin hosts a diverse array of bacteria, fungi, and viruses that form its microbiota. These microbes are crucial for maintaining skin homeostasis by protecting against pathogens, stimulating the immune system, and breaking down natural host products. Microbial populations are organized into complex communities that significantly influence the functionality of healthy skin. When the microbiota is disrupted, it can adversely affect the skin's immune homeostasis and contribute to systemic diseases (Willmott et al., 2023).

The skin primarily hosts four main bacterial phyla; Actinobacteria, Firmicutes, Proteobacteria, and Bacteroidetes. In moist regions, Staphylococcus and Corynebacterium are the most prevalent. Oily areas tend to exhibit less diversity, with Cutibacterium being the dominant species. In contrast, dry areas of the skin show the greatest diversity, consisting of a wide range of these four phyla (Smyth & Wilkinson, 2023).

What is the relationship between UV and the Skin Microbiome

As a unique ecosystem, human skin and its microbial inhabitants are also influenced by external environmental stressors, including UVR (Burns et al., 2019). UVR can directly or indirectly affect the skin microbiome. Studies have shown changes in the composition of the skin microbiome, with different bacteria responding differently to UVA and UVB radiation (Gilaberte et al., 2024).

A study published in 2023 found significant changes in microbial beta diversity after four weeks of extensive sunlight exposure on the forearms of participants, compared to baseline measurements. Prior to taking a holiday in a sunny destination (minimum of 7 days duration), volunteers had skin swabs taken from their extensor forearm (d0), and upon their return, skin swabs were repeated at d1, d28, and d84. This suggests that sun exposure influences the diversity and composition of the skin microbiota (Willmott et al., 2023). Additionally, the overall composition of the skin microbiome may be altered long-term following exposure to UVA and UVB radiation on the backs of the volunteers. Notable increases were observed in Cyanobacteria spp., Fusobacteria spp., Verrucomicrobia spp., and Oxalobacteraceae spp. In contrast, Lactobacillaceae spp. and Pseudomonadaceae spp. decreased, with a more pronounced decline following UVA exposure (Burns et al., 2019). 

Research indicates that, similar to skin cells, bacteria respond differently to the UVA and UVB components of UVR. One study examining the effects of UVR on Pseudomonas aeruginosa found that both UVA and UVB contribute to bacterial inactivation, shedding light on the vulnerability of specific microorganisms to UVR. Another study compared the responses of P. aeruginosa to those of Escherichia coli under similar conditions. While UVA significantly impacted the viability of P. aeruginosa, it had little to no observable effect on E. coli (Smith et al., 2023).

UVR, Skin Microbiome, and Immune System Interaction

The effects of UVR on the skin microbiome can occur through both direct and indirect mechanisms. UVR presents an immediate threat to both mammalian and microbial cells. Additionally, UVR can alter the microbial habitat of exposed skin, leading to further changes in the skin microbiome. One indirect mechanism involves the increased expression of antimicrobial peptides (AMPs) by the skin in response to UVR. Some species within the skin microbiome exhibit resistance to UVR, such as Micrococcus luteus, which utilizes carotenoid pigments and has high endonuclease activity to counteract the otherwise bactericidal effects of UVR (Smith et al., 2023).

At sub-toxic levels, UVR can trigger a pathogen/damage-associated molecular pattern (PAMP/DAMP) response. This response may result in the release of microbial signals like oleic acid, lipopolysaccharides (LPS), and porphyrins, which can alter immune signaling and promote inflammation (Patra, Byrne & Wolf, 2016).

Microbial metabolites can influence dendritic cells, aiding in the recognition and capture of pathogens. Additionally, microorganisms can produce natural antimicrobial peptides (AMPs) or regulate their production in keratinocytes, with UVR exposure potentially enhancing AMP levels. The UVR-induced cis-UCA may not only lead to an altered immune response but could also indirectly modify the microbial load by affecting the skin's microenvironment through unknown mechanisms. Furthermore, the microbiome can induce complement and interleukin-1 (IL-1) in response to UVR stress, influencing skin immunity through various cytokines, particularly in the Th17 pathway. Consequently, the production of IL-17 by keratinocytes may lead to changes in AMP production, creating a loop that ultimately affects the microbiome (Figure 2) (Patra, Byrne & Wolf, 2016).

UVR can weaken the body's immune response to infectious microorganisms, potentially increasing the risk of microbial infections or elevating existing ones. This occurs as UVR induces dysbiosis, disrupting the natural balance of the skin microbiome and altering skin homeostasis. When the protective microbial community is compromised, harmful pathogens may thrive, leading to higher susceptibility to infections. Additionally, the changes in immune signaling pathways caused by UVR can impair the skin's ability to defend against these pathogens, further heightening the risk of skin-related infections and inflammatory conditions. Understanding this interplay emphasizes the importance of protecting the skin from excessive UV exposure to maintain both skin health and overall immune function (Gilaberte et al., 2024).

Figure 2:  Possible mechanisms microbes can influence UV-induced immune suppression. Image taken from (Patra, Byrne & Wolf, 2016).

Some fungi display photomorphogenic effects when exposed to UV light. A study found that increased doses of UV radiation reduced the production of porphyrins by Cutibacterium acnes, showing that these facial bacteria respond to UV exposure. They noted that C. acnes reacted to UV-B at doses lower than 20 mJ/cm², even before any significant skin damage occurred (Wang et al., 2012).

Malassezia spp., part of the normal skin flora, can cause pityriasis versicolor, a common skin condition mainly in tropical areas. At the typical sites of this condition, sunburn is rarely triggered. Malassezia furfur produces a UV-filtering compound known as pityriacitrin, which is believed to offer protective benefits. However, UVR is also known to suppress the cellular growth of Malassezia furfur (Patra, Byrne & Wolf, 2016).

Sunscreen, UV, and Skin Microbiome

In recent years, effective sun protection strategies have been developed, emphasizing personalized approaches like wearing sun-protective clothing and using sunscreen. Modern sun protection products feature photostable, broad-spectrum UVA/UVB filters to protect against sunburn, skin cancer, photodermatoses, and photoaging. Many also include active ingredients that help prevent hyperpigmentation and premature skin aging, extending protection beyond just UV radiation (Schuetz et al., 2024).

There have been recent questions about how sunscreen affects the skin microbiome, though limited research is available. Nanoparticles like coated titanium dioxide (TiO₂) and zinc oxide (ZnO) in sunscreens have been shown to have antimicrobial effects, due to their ability to release metal ions and generate reactive oxygen species (ROS). The impact of these nanoparticles varies depending on the microorganism. Coated TiO₂ does not significantly affect skin bacteria growth, while UV exposure increases the bactericidal activity of uncoated ZnO. Most sunscreens use coated ZnO and TiO₂ particles, which are less harmful to bacteria (Grant et al., 2024). 

Factors like particle size, pH, preservatives, and added antimicrobial compounds in sunscreens may also influence the skin microbiome. Organic UV filters have been found to inhibit the growth of marine bacteria, fungi, and fish gut microbiota, but their direct effect on human skin bacteria is less known (Grant et al., 2024).

Study: Sunscreens can preserve human skin microbiome upon erythemal UV exposure (Schuetz et al., 2024)

In the above study they compared the effect of sunscreen SPF20 and placebo on UV exposed skin. Erythema was prominently observed in the unprotected areas, partially in the placebo treated zones, but was absent in the SPF20 treated areas, indicating effective photoprotection from the SPF (Schuetz et al., 2024).

The In vitro results found that L. crispatus was one of the most affected microbes when sunscreen was applied, showing a positive association with its abundance. In contrast, Cutibacterium acnes did not show significant changes in its relative abundance. UV exposure reduced the ratio of Lactobacillus to Cutibacterium, indicating more Cutibacterium in those areas, while the sunscreen helped restore the original balance between these two types of bacteria (Schuetz et al., 2024).

L. crispatus is common in the skin microbiome of younger individuals (18-35 yrs) and is also prevalent in the vaginal microbiome, playing an important role in women's health (Garlet et al., 2024) (Schuetz et al., 2024) (Argentini et al., 2022). 

Certain microorganisms, like L. crispatus, benefit from extra UV protection, as mentioned in the above clinical study. To confirm these results, they developed an in vitro model using individual bacteria and UV filters. They tested the survival of Lactobacillus crispatus, Cutibacterium acnes, and Staphylococcus epidermidis under UV stress (Schuetz et al., 2024).

The results showed that specific UV filters, such as octocrylene and zinc oxide, improved the survival of L. crispatus compared to the control. Combinations of these filters also protected L. crispatus, similar to the in vivo findings. However, some filters, like butyl methoxydibenzoylmethane, reduced the population of C. acnes, while maintaining or increasing S. epidermidis levels. This suggests that choosing the right UV filters in sunscreens is very important (Figure 3) (Schuetz et al., 2024).

In conclusion, the above study provided valuable insights into the protective effects of an SPF 20 sunscreen on the skin microbiome after UV exposure. The findings highlight the relationship between UV radiation and the skin microbiome, emphasizing the importance of sun protection for maintaining healthy skin (Schuetz et al., 2024).

In the test, various UV filter formulations showed different effects on microbial survival. For example, some filters improved the survival of Lactobacillus crispatus, while others reduced Cutibacterium acnes (Schuetz et al., 2024).

Despite limitations due to the small number of volunteers and sample variability, there results suggest that applying sunscreen before UV exposure can be beneficial for the skin microbiome. The researchers also believe that sunscreens with higher SPF values may offer even greater protection (Schuetz et al., 2024).

Lactobacillus crispatus, may help protect the skin and support its immune response, similar to its role in vaginal health. The ability of select UV filters to preserve beneficial bacteria while reducing harmful C. acnes could lead to new skincare products aimed at protecting both skin and its microbiome from UV stress, enhancing overall skin resilience (Schuetz et al., 2024).

Figure 3: The survival rates of each microbial population four hours after exposure were calculated as a percentage compared to the initial population, with the relative protection provided by the UV filters expressed as a percentage. Image taken from (Schuetz et al., 2024).

Probiotics for Protecting Your Skin Microbiome from UV Damage 

Probiotics are live microorganisms that provide health benefits to the host when consumed in sufficient amounts. Certain strains of lactic acid bacteria have been found to positively influence gut microbiota composition and metabolism, and in some cases, they can inhibit the growth of harmful bacteria. Research has shown a link between the gut-immune axis and skin health, with probiotic-rich foods helping to maintain skin balance and support the immune system (Souak et al., 2021).

Probiotics have also shown potential in protecting against UV-induced skin damage. For example, Lactobacillus johnsonii NCC 533 (La1) has been found to help stabilize the skin's immune system by preventing UV-induced increases in interleukin-10 and reducing the recruitment of Langerhans cells. Similarly, Lactobacillus rhamnosus GG (LGG) has been shown to prevent UV-related skin tumors due to its lipoteichoic acid (LTA), a component of gram-positive bacteria cell walls (Souak et al., 2021). 

Other potential probiotic candidates for photoprotection include Lactobacillus plantarum HY7714, Bifidobacterium breve, and Bifidobacterium longum (Souak et al., 2021).

Conclusion

In conclusion, protecting both the skin and its microbiome can help lower the risk of imbalances caused by UVR. Using sunscreens not only provides effective sun protection but also strengthens the skin barrier, which may help preserve a healthy microbiome by minimizing the penetration of harmful UV rays and environmental stress (Gilaberte et al., 2024).

More studies need to be done to understand how different wavelengths of UVR affect the skin microbiome, as well as the long-term impact of UVR on skin health, including its role in chronic conditions and aging. Additionally, further research is needed to explore how sunscreens influence the microbiome and more high-quality clinical studies are essential to confirm the potential of these approaches in safeguarding the skin microbiome from the effects of solar radiation (Gilaberte et al., 2024).

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