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Pistone, D. Skin Microbiome. Encyclopedia. Available online: https://encyclopedia.pub/entry/14394 (accessed on 20 June 2024).
Pistone D. Skin Microbiome. Encyclopedia. Available at: https://encyclopedia.pub/entry/14394. Accessed June 20, 2024.
Pistone, Dario. "Skin Microbiome" Encyclopedia, https://encyclopedia.pub/entry/14394 (accessed June 20, 2024).
Pistone, D. (2021, September 22). Skin Microbiome. In Encyclopedia. https://encyclopedia.pub/entry/14394
Pistone, Dario. "Skin Microbiome." Encyclopedia. Web. 22 September, 2021.
Skin Microbiome
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Our body is home to a complex community of microorganisms that help us maintain homeostasis and prevent colonization from pathogens. This residential community is known as the microbiota (often incorrectly used as a synonym for microbiome), referring to all the microorganisms, including archaea, bacteria, eukaryotes (fungi and yeasts, protists), viruses, and bacteriophages that colonize and inhabit a specific niche of our body. Instead, the microbiome describes the entire set of genomes and microbial genes found in a specific microbiota. The human skin microbiota is essential for maintaining homeostasis and ensuring barrier functions. Over the years, the characterization of its composition and taxonomic diversity has reached outstanding goals, with more than 10 million bacterial genes collected and cataloged.

skin microbiota skin sampling techniques NGS culturomics

1. Introduction

Our body is home to a complex community of microorganisms that help us maintain homeostasis and prevent colonization from pathogens [1][2]. This residential community is known as the microbiota (often incorrectly used as a synonym for microbiome), referring to all the microorganisms, including archaea, bacteria, eukaryotes (fungi and yeasts, protists), viruses, and bacteriophages that colonize and inhabit a specific niche of our body. Instead, the microbiome describes the entire set of genomes and microbial genes found in a specific microbiota [1][2][3]. Site-specific microbial communities colonize different anatomical niches of the human body (e.g., the skin, gut, oral cavity, nasal cavities, and urogenital tract). In 2007, the U.S. National Institutes of Health (NIH) started the “Human Microbiome Project” (HMP), a two-phase project to (a) produce the reference genome sequences for at least 900 bacteria, (b) catalog microbial genome sequences, and (c) help researchers in metagenomic data management [4]. The initial stage of the project, called the Human Microbiome Project 1 (HMP1), which was established in 2008 and completed in 2013, aimed to characterize the microbial communities from 300 healthy patients across five different anatomical sites (i.e., the gastrointestinal tract, urogenital tract, skin, nasal cavities, and oral cavity) [4]. The second stage, called the Integrative Human Microbiome Project (iHMP or HMP2), was designed to characterize in more detail the host-microbiome interactions, focusing on three conditions: pregnancy and pre-term birth, the onset of inflammatory bowel diseases (IBD), and the onset of type II diabetes [5]. Specifically, concerning the skin microbiome, the characterization of its diversity has reached outstanding goals over the years. For example, consortia such as the integrated Human Skin Microbial Gene Catalog (iHSMGC) collected and cataloged more than 10 million genes [6], an impressive task to have accomplished, and included a high number of individuals in the study, applying Next Generation Sequencing (NGS) technology and huge computing power. Nevertheless, the study of the skin microbiota presents specific challenges to consider when designing a study.

2. The Skin Microbiota

As the most exposed organ of our body, with an estimated surface area of about 1.8 m2 (even larger when considering follicular structures and other appendages), the skin is inhabited by more than one million bacteria/cm2 co-participating in maintaining the physical barrier function to the external environment and preventing the penetration and invasion of pathogens [2][3][7][8]. Besides its protective function, the skin plays an essential role in thermoregulation processes and vitamin D synthesis [9]. However, rather than a barricade that separates us from the bacterial community living on us, the skin should be regarded as a wide and dynamic interface on which the microbiota cooperates with the immune system in a modulatory activity that is crucial for our health [10][11][12].
The human skin can roughly be grouped into three main physiological types: (1) oily/sebaceous areas (i.e., forehead, upper back, and nose); (2) dry areas (i.e., forearm and lower back); (3) moist areas (i.e., armpits, backs of knees, nostrils, and groin). Specific bacterial taxa inhabit these different cutaneous micro-environments: Cutibacterium and Propionibacterium have a clear preference for sebaceous niches, whereas the genera Staphylococcus and Corynebacterium tend to colonize moist zones, and Proteobacteria and Flavobacteriales thrive in dry sites [13]. The same area can also be deeply affected by lipid and water levels; for example, sebum concentration of the cheek, but not the forehead, is significantly correlated with microbial composition and diversity and, on the contrary, the hydration level of the forehead was found to be a good predictor of nature and diversity of this site-specific microbiota [14].
Many of the skin commensals generally found on healthy human skin belong to four phyla: Actinobacteria (Corynebacterium, Propionibacterium, Cutibacterium, Micrococcus, Actinomyces, Brevibacterium), Firmicutes (Staphylococcus, Streptococcus, Finegoldia), Proteobacteria (Paracoccus, Haematobacter), and Bacteroidetes (Prevotella, Porphyromonas, Chryseobacterium).
Coagulase-negative staphylococci (CoNS) such as Staphylococcus epidermidis and Staphylococcus hominis are among the most common Gram-positive species inhabiting the human skin [15]. These bacteria, previously considered innocuous, have an active role in contrasting the colonization of Staphylococcus aureus and other pathogens but are now regarded as important opportunistic pathogens as well [16][17]. Indeed, S. epidermidis and other CoNS can frequently cause nosocomial and neonatal infections and colonize prosthetics and other medical devices [18][19]. Moreover, CoNS can cause debilitating and difficult-to-eradicate infections that are causing medical concern due to their biofilm formation propensity and their role as reservoirs of antibiotic-resistant genes [20]. Another ubiquitous inhabitant of the human skin is Cutibacterium acnes (formerly Propionibacterium acnes), a Gram-positive facultative anaerobe with a lipophilic attitude that tends to colonize the pilosebaceous unit [21]. Different strains of C. acnes have been previously implicated in a plethora of diseases, including acne (see below). Its role as an opportunistic pathogen, especially in post-surgery wound infections, is becoming more prominent as well [22][23][24].
Archaea enclose up to 4% of the entire microbial diversity of the skin [25][26]. The Thaumarchaeota phylum is one of the most abundant, and its members could be implicated in ammonia oxidation processes [26]. In the complex human skin ecosystem, even the presence of mites, especially Demodex spp. as ubiquitous ectoparasites of the pilosebaceous unit, is common, and their possible pathogenic role is highly debated [27]. Indeed, even if the causal relationship between the abundance of Demodex spp. and a specific skin-associated disease has not been clarified yet, the high density of these parasites has been tentatively associated with some inflammatory conditions such as rosacea, blepharitis, perioral, and seborrheic dermatitis or chalazion [28][29][30]. Healthy human skin also harbors resident and transient viruses such as cutaneous beta and gamma human papillomaviruses, commonly found in many individuals [31][32]. Although low in biomass and probably one of the most understudied communities on the skin, bacteriophages can deeply influence the microbiota diversity and its physiological activity [33].
The amount of skin bacteria on humans is relatively high, and they are constantly shed in the surrounding environment together with dead cells of the stratum corneum of the skin, so the fact that they are often the major microbial component in the air, soil, and other surfaces in a crowded urban area is not surprising [34][35].
The constant crosstalk between the skin immune system and the cutaneous microbiota acts as a powerful pathogen control system [1][3]. However, under some circumstances, for example, when the defensive skin barrier is compromised or a disequilibrium between commensal bacteria and pathogens occurs, skin diseases can arise [2][3].
Aging is another key factor causing critical changes in the skin microbiota. Some authors have reported increased species diversity in the skin microbial community of elderly people [36][37][38], although conflicting results have also been published [39]. Interestingly, it has been shown that data from skin microbiota can be used to predict age more accurately than gut or oral microbiota [40].
Skin aging is a process that induces alterations in skin structure and physiology, with a decrease in hydration levels, the appearance of hyperpigmented spots and wrinkles, and modified sebaceous gland activity [41]. In particular, the reduction in sebum production may reduce nutrients for commensal bacteria and favors the colonization of opportunistic species. Several studies reported a reduction in the dominant genus Cutibacterium and a parallel increase in the relative abundance of Corynebacterium and some Proteobacteria on different skin sites in older groups [36][37]. The fungal diversity of the genus Malassezia is also known to experience age-related changes, with older individuals showing Malassezia sympodialis as the predominant species [42]. The prevalence of Demodex increases with age as well. In this respect, it has been reported that Corynebacterium kroppenstedtii-like OTUs tend to replace other Corynebacterium OTUs in older adults [43]. The relationship between these skin-inhabiting mites and their main symbionts might deserve further attention (see below).
The use of cosmetics can also boost bacterial diversity on the skin, with an increase in genera such as Ralstonia spp., which have been tentatively linked to the ability to metabolize xenobiotics [44][45].
Historically, microbiology has always explored microbial skin communities using culture-dependent approaches and studying individual species as isolated units [3][46]. The fundamental limit in this targeted approach is the selection and isolation of only the culturable fraction of the microbiota (focusing on bacteria), which represents a small part of the entire skin microbial diversity [47]. Indeed, the vast majority of skin commensal bacteria remains unculturable or difficult to cultivate (see below), a sign of a highly diversified bacterial community with specific growing requirements [1][48][8][49][50]. The great opportunities offered by culture-independent methods were already clear several decades ago, at the beginning of the PCR era, but technology started a real revolution in the field with the advent of NGS platforms only in the most recent years. From the first study by Woese (1977), in which they used the 16S rRNA gene to investigate the phylogeny of prokaryotes [51], the advancements of molecular biology-based techniques from the Sanger method up to the latest high throughput NGS technologies have rapidly provided new possibilities to increase the level of microbiome characterization. These studies commonly use two main NGS approaches—amplicon sequencing and whole-genome shotgun sequencing [2] (see Section 4). Despite the detailed picture of the microbial community composition obtained with these methods, elucidating the role of the skin microbiota in different diseases will also require the application of other techniques (derived from metatranscriptomics, metaproteomics, and metabolomics), to investigate gene expression profiles and metabolic byproducts [52].

2.1. Resident and Transient Skin Microbiota

The human skin microbiota is characterized by a rather high degree of temporal variability, especially when compared to more stable microbial communities, such as those localized in the gut or the mouth [53]. High-resolution time-series studies, following the composition of the individual skin microbiota over time, have determined the absence of a highly abundant core microbiota, although some taxa can be rather persistent [54][55]. All areas protected or less exposed to the external environment, such as the external auditory canal (inside the ear), the nare (inside the nostril), and the inguinal crease, were shown to be more consistent over time [13]. As a general rule, sites harboring a greater diversity of microorganisms tend to be less stable over time in terms of community members and bacterial composition; these sites include the volar forearm (forearm), the popliteal fossa, the antecubital fossa, the plantar heel (the bottom of the heel of the foot) and the interdigital web space (between the fingers) [13].
Skin microorganisms can be classified into resident and transient, even if defining a clear edge is difficult. For facilitating classification into these two categories, one criterion could be that transient microbes can be permanently removed by applying detergent and disinfectant agents, or soap and water [56][57]. Another classification approach, practical and straightforward, identifies the commensal and symbiotic microbiota with the ‘normal’ and resident component, whereas the pathogens, supposedly derived from the environment, would constitute the transient part [8]. According to the circumstances, several skin microorganisms can act either as commensal or pathogenic, adding a further level of complexity. The fact that the skin, particularly the epidermis, is directly exposed to the external environment can also be considered a confounding factor in the resident/transient distinction.
Resident skin bacteria play a series of essential functions, such as the inhibition and control of pathogens (and other transient bacteria) through the production of antimicrobial metabolites and the modulation and training of the immune system. Indeed, the dynamic equilibrium between commensal, opportunistic, and pathogenic species remains a fundamental factor in skin homeostasis and health.
Transient bacteria, deriving from other body sites, direct skin contact, or indirect sharing of objects and tools, can temporarily colonize the skin since they might not reproduce due to the inhibiting action of permanent microbiota. Persistent contamination from environmental bacteria can be a serious issue to resolve when trying to characterize the resident skin microbiota, especially for low-abundance taxa, but longitudinal and comparative studies can solve this problem.
A healthy skin microbial community tends to be relatively stable over long periods of time, and it is also known to return rapidly to its original state after environmental perturbations. However, simple routine actions, such as applying perfumes or cosmetics or swimming in seawater, can deeply affect and change the composition of the bacterial skin community for hours or even days [58][59].
NGS technology and molecular analyses allow for investigating such temporal and spatial variability under the circumstances previously mentioned—that is, changing abiotic factors, disruption of the residential microbial community, and temporal colonization of transient environmental microbes [60].

2.2. Insight into the Core Microbiota of Derma and Adnexal Structures

The skin is a complex structure, and so far, the focus of this paper has been on the epidermis. Under the most superficial layer, the derma constitutes a connective tissue-rich stratum laying on the subcutaneous tissues. The derma is more heterogeneous than the epidermis and rich in secondary structures, such as hair follicles, sweat glands, sebaceous glands (oil glands), apocrine glands, lymphatic vessels, nerves, and blood vessels.
The dermis (the skin tissue underlying the epidermis) microbiota presents distinctive features compared to the superficial microbial community. The microbiota living in the deeper layer of the skin is reported to be quantitatively and qualitatively limited, with a tendency towards stability and, in general, more conserved among different individuals [61]. Generally, it primarily consists of a subset of the entire bacterial diversity reported in the superficial layers of the skin [61]. Microbes inhabiting the dermis might also have an essential role in replenishing the bacterial surface population as skin flakes off or in the process of skin recolonization after environmental shocks. Nevertheless, part of the typical microbiota inhabiting the epidermis, for example, staphylococcal species, might induce inflammation once penetrating the dermis or lower layers of the skin [62].
For a long time, the derma was considered sterile and not inhabited by bacteria or other microorganisms and regarded as a hostile environment. However, on the contrary, this body niche can offer several resource-rich environments for fungi and bacteria, such as the hair follicles and the eccrine and apocrine glands [61].
The pilosebaceous unit, particularly the sebaceous follicle, is a lipid-rich niche inhabited mainly by Cutibacterium acnes (>90%), some species belonging to the genera Corynebacterium spp. and Staphylococcus spp. (circa 5%), and Malassezia spp. fungi. The follicular opening and the upper part of the hair follicle present more variability, either in species or abundance, compared to the lower layers.
Scalp hair follicles, which are rich in sebum produced by sebaceous glands, are also colonized by Cutibacterium spp. (mainly C. acnes) and staphylococci (mainly S. epidermidis), which can alone make up more than 90% of the gene sequencing in scalp microbiota studies [63]. Malassezia spp. and Corynebacterium spp. represent other important components of the scalp microbiota that benefit from lipids of the sebum. The remaining part of the microbiota consists of less numerous species belonging to Streptococcus spp., Acinetobacter spp., and Prevotella spp. [64][65].
The microbiota of the hair and fingernails, highly keratinized structures, is highly variable among human beings, but the presence of unique individual signatures might have applications in forensic science [66]. Moreover, fingernails can be easily colonized by a range of microbes, including pathogens that can represent a possible source of infection [67][68][69].

2.3. Dysbiosis of the Skin Microbiota in Specific Diseases

The etiology and development of skin diseases are complex processes influenced by diet, metabolites, pathogens, immune system response, skin and gut microbiota alterations [70][71]. We have summarized the characteristics of some well-studied skin diseases in a table (Table 1), highlighting specific taxonomic changes in microbiota composition and other factors tentatively associated with each pathology.
Table 1. Microorganisms and other factors associated with skin diseases.
Skin Disease Microorganisms References Other Factors Implicated in the Pathology Moderately Associated (•)
Highly Associated (•••)
Rosacea Demodex folliculorum [72][73][74][75][76][77] Microbiome composition •••
Helicobacter pylori [78][79] Solar exposure •
Staphylococcus epidermidis [74][80] Dietary agents •
Chlamydophyla pneumoniae [81][82] Drugs •
Bacillus oleronius [74] Abnormalities of the cutaneous vascular and lymphatic system •
    Enhanced expression of toll-like receptor 2 in the epidermis and amplified inflammatory response •••
    Abnormalities of the sebaceous gland •
    Dermal matrix degeneration •
Atopic dermatitis Staphylococcus aureus [83][84][85][86][87] Food allergies •
herpes simplex virus ↑ [88][89] Irritants in contact with skin •
(clothes, detergents, jewelry, ets)
Staphylococcus epidermidis
CoNS
[88] Hormonal changes •
    Decrease in antimicrobial peptides •
    Increased skin pH •
    Th2 (cytokines such as IL-4 and IL-13) •
Psoriasis Staphylococcus aureus [90][91][92][93][94][95] Genetics •••
Streptococcus pyogenes secondary colonization? Hormonal changes •
Human papillomavirus and endogenous retroviruses ↑   Immune disorders •
Malassezia spp. ↑   Alcohol consumption •
Candida albicans   Smoking •
Propionibacterium spp. ↓ [93][94] Stress •
Acne vulgaris Cutibacterium acnes [96][97] Hormonal changes •••
Malassezia spp. ↑ [98] Medications (e.g. corticosteroids, lithium) •
    Diet •
    Stress •

We reported the main cutaneous diseases in the first column of the table. A list of the main bacteria associated with the diseases can be found in the second column (the arrows ↑ and ↓ indicate and over or under representation of the microorganisms in the affected skin). References regarding disease-associated bacteria are reported in line with corresponding bacteria type. In the last column, we added a list of other factors putatively involved, with different importance, in the etiology and development of the diseases.

2.3.1. Acne Vulgaris

Acne vulgaris is a skin lesion affecting more than 9% of the human population, with higher prevalence (up to 80–90%) in adolescents and young adults [99][100][101]. This skin condition is caused by the obstruction and inflammation of the pilosebaceous units, which can result in the formation of comedones, papules, pustules, nodules, and cysts [102]. The pathophysiology of acne vulgaris is somewhat complex, and multiple studies suggested that strains of C. acnes and Malassezia sp. are implicated in its development [103]. The biosynthesis of vitamin B12 by C. acnes has been hypothesized to have a role in the pathogenesis of acne; an increase in vitamin B12 might cause a concomitant production of porphyrins promoting inflammation [104]. Other biological factors might be triggering acne vulgaris, and thus, the roles of the host immune response and other members of the microbiota remain to be adequately defined [105]. When comparing the microbiota of the skin surface and follicles, the main bacterial and fungal species are present in both niches, and commonly detected with different sampling and sequencing methods; higher diversity and site specificity are reported for viruses on the skin surface.

2.3.2. Atopic Dermatitis

Atopic dermatitis (AD) is a chronic skin alteration that can manifest in different body sites and is characterized by dry, itchy skin patches and relapsing eczema [106]. This condition affects 15–20% of children, with a lower prevalence (3%) in adults [107][108]. Low bacterial diversity is frequently reported in AD, and cutaneous microbiota dysbiosis might be a driving factor in eczema pathogenesis. In particular, changes include depletion of Malassezia spp., high non-Malassezia fungal diversity associated with the relative abundance of S. aureus (strongly associated with AD) and S. epidermidis, and the reduction of other genera, such as Propionibacterium [106][109][110][111]. Opportunistic viral, bacterial, and fungal infections are often reported in patients with AD; dry skin and compromised microbiota might also be more susceptible to pathogen colonization and successful establishment. In addition to cutaneous dysbiosis, gut dysbiosis has also been observed in AD [112][113], especially in infants, [114], although taxa specifically under- or over-represented varied among the studies, with conflicting results [113].
The establishment of altered gut microbiota with AD seems to occur in the early stages of development, as demonstrated by studies showing that atopic infants vs. non-atopic infants at 1 year of age had different gut compositions at 3 weeks of age [115]. The majority of the evidence derived from molecular data suggests that gut colonization occurs through contamination shortly after delivery [116][117]. At about 2.5 years of age, the composition, diversity, and functions of the infant microbiota resemble those of the microbiota of adult people [118]. This has caused researchers to become interested in shaping gut microbiota in the early stages to prevent the development of allergic diseases later in life with strategies based on the use of probiotics (see below).

2.3.3. Psoriasis

Psoriasis is an idiopathic skin disorder affecting approximately 1–2% of the human population [119][120]. The disease is characterized by a chronic inflammatory condition that can manifest into hyperkeratosis, hyperproliferation of keratinocytes, infiltration of the skin by immune cells, and angiogenesis [121]. Skin lesions from these patients had higher bacterial diversity compared to healthy individuals, with increased Streptococcus and significantly less C. acnes [122]. S. aureus has long been regarded as associated with psoriasis, but the psoriasis microbiome has not been clearly defined yet, and the roles of other components of the microbiota remain to be elucidated.

2.3.4. Rosacea

Rosacea is an inflammatory dermatosis of the facial skin affecting roughly 10% of the population (estimates can be rather variable, between 5% and 46%), and characterized by flushing, redness, papules, and pustules, for which pathogenesis remains largely unknown [123][124][125]. The majority of researchers distinguish between rosacea-like demodicosis and papulo pustular rosacea, with the first one presenting a higher density of Demodex mites. However, in a recent study, no clear differences were found between the two conditions, and the authors suggested considering the two entities as different phenotypes of the same disease [73]. Several bacteria, such as S. epidermidis, Helicobacter pylori, Chlamydophila pneumoniae, and Bacillus oleronius, were also considered associated with the disease [126]. Colonization with Demodex folliculorum and Demodex-associated bacteria (based on 16S rRNA gene sequencing) also positively correlates with disease severity [127]. As stated above, Demodex spp. are the most complex members of the human skin microbiome; they are mostly commensals, although a pathophysiological role in inflammatory dermatoses is recognized. Recently, there has been an interest in screening them for the presence of endosymbionts, which are rather common in different species of mites (and, in general, arthropods), where they play key roles in biological and physiological processes and can be the target of potential medical and therapeutical applications [128][129]). In Demodex spp., different species of the genus Bacillus (Bacillus oleronius, Bacillus simplex, Bacillus cereus, and Bacillus pumilus) have been considered presumed symbionts [130]. However, currently, Corynebacterium kroppenstedtii subsp. demodicis is the only bacterium for which a role as the primary endosymbiont of Demodex folliculorum is well supported by the following evidence: (a) the bacteria are vertically transmitted; (b) they are present in all individuals of the species and located in a well-defined structure in the mite opisthosoma; (c) they supposedly participate in lipid metabolisms by providing lipid-digesting enzymes [131].
Since endosymbiont removal is known to have negative effects on the host fitness, a better understanding of this relationship could have important implications for Demodex spp. density and the treatment of rosacea and other skin conditions.

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