Neutral Processes Drive Seasonal Assembly of the Skin Mycobiome

ABSTRACT The importance of microorganisms to human skin health has led to a growing interest in the temporal stability of skin microbiota. Here we investigated the dynamics and assembly of skin fungal communities (mycobiomes) with amplicon sequencing of samples collected from multiple sites on 24 healthy Chinese individuals across four seasons (in the order of winter, spring, summer, and autumn in a calendar year). We found a significant difference in community compositions between individuals, and intrapersonal community variation increased over time at all body sites. Within each season, the frequency of occurrence of most operational taxonomic units (OTUs) was well fitted by a neutral model, highlighting the importance of stochastic forces such as passive dispersal and ecological drift in skin community assembly. Despite the significant richness contributed by neutrally distributed OTUs, skin coassociation networks were dominated by taxa well-adapted to multiple body sites (forehead, forearm, and palm), although hub species were disproportionately rare. Taken together, these results suggest that while skin mycobiome assembly is a predominantly neutral process, taxa that could be under the influence of selective forces (e.g., host selection) are potentially key to the structure of a community network. IMPORTANCE Fungi are well recognized members of the human skin microbiota and are crucial to cutaneous health. Common cutaneous diseases such as seborrheic dermatitis and dermatophytes are linked to fungal species. Most studies related to skin microbial community dynamics have focused on Western subjects, while non-Western individuals are understudied. In this study, we explore the seasonal changes of the skin mycobiome in a healthy Chinese cohort and identify ecological processes that could possibly give rise to such variations. Our work reveals the dynamic nature of host skin fungal community, highlighting the dominant roles neutral forces play in the seasonal assembly of skin mycobiome. This study provides insight into the microbial ecology of the human skin microbiome and fills a knowledge gap in the literature regarding the dynamics of skin fungal community.

Download Full-text

Complete Genome Sequence of Malassezia restricta CBS 7877, an Opportunist Pathogen Involved in Dandruff and Seborrheic Dermatitis

Microbiology Resource Announcements ◽

10.1128/mra.01543-18 ◽

2019 ◽

Vol 8 (6) ◽

Cited By ~ 4

Author(s):

Stanislas C. Morand ◽

Morgane Bertignac ◽

Agnes Iltis ◽

Iris C. R. M. Kolder ◽

Walter Pirovano ◽

...

Keyword(s):

Human Skin ◽

Genome Sequence ◽

Complete Genome Sequence ◽

Complete Genome ◽

Seborrheic Dermatitis ◽

Skin Microbiome ◽

Basidiomycetous Yeasts ◽

Content Type ◽

Opportunist Pathogen ◽

Malassezia Restricta

Malassezia restricta, one of the predominant basidiomycetous yeasts present on human skin, is involved in scalp disorders. Here, we report the complete genome sequence of the lipophilic Malassezia restricta CBS 7877 strain, which will facilitate the study of the mechanisms underlying its commensal and pathogenic roles within the skin microbiome.

Download Full-text

Temporal Stability of the Healthy Human Skin Microbiome Following Dead Sea Climatotherapy

Acta Dermato Venereologica ◽

10.2340/00015555-2769 ◽

2018 ◽

Vol 98 (2) ◽

pp. 256-261 ◽

Cited By ~ 8

Author(s):

M Brandwein ◽

G Fuks ◽

A Israel ◽

A Al-Ashhab ◽

D Nejman ◽

...

Keyword(s):

Human Skin ◽

Temporal Stability ◽

Dead Sea ◽

Skin Microbiome ◽

Healthy Human

Download Full-text

Features of the Skin Microbiota in Common Inflammatory Skin Diseases

Life ◽

10.3390/life11090962 ◽

2021 ◽

Vol 11 (9) ◽

pp. 962

Author(s):

Iva Ferček ◽

Liborija Lugović-Mihić ◽

Arjana Tambić-Andrašević ◽

Diana Ćesić ◽

Ana Gverić Grginić ◽

...

Keyword(s):

Skin Diseases ◽

Seborrheic Dermatitis ◽

Bacterial Species ◽

Clinical Manifestations ◽

Skin Microbiome ◽

Bacterial Strains ◽

Skin Microbiota ◽

Inflammatory Skin Diseases ◽

Bacterial Microbiome ◽

Inflammatory Skin

Many relatively common chronic inflammatory skin diseases manifest on the face (seborrheic dermatitis, rosacea, acne, perioral/periorificial dermatitis, periocular dermatitis, etc.), thereby significantly impairing patient appearance and quality of life. Given the yet unexplained pathogenesis and numerous factors involved, these diseases often present therapeutic challenges. The term “microbiome” comprises the totality of microorganisms (microbiota), their genomes, and environmental factors in a particular environment. Changes in human skin microbiota composition and/or functionality are believed to trigger immune dysregulation, and consequently an inflammatory response, thereby playing a potentially significant role in the clinical manifestations and treatment of these diseases. Although cultivation methods have traditionally been used in studies of bacterial microbiome species, a large number of bacterial strains cannot be grown in the laboratory. Since standard culture-dependent methods detect fewer than 1% of all bacterial species, a metagenomic approach could be used to detect bacteria that cannot be cultivated. The skin microbiome exhibits spatial distribution associated with the microenvironment (sebaceous, moist, and dry areas). However, although disturbance of the skin microbiome can lead to a number of pathological conditions and diseases, it is still not clear whether skin diseases result from change in the microbiome or cause such a change. Thus far, the skin microbiome has been studied in atopic dermatitis, seborrheic dermatitis, psoriasis, acne, and rosacea. Studies on the possible association between changes in the microbiome and their association with skin diseases have improved the understanding of disease development, diagnostics, and therapeutics. The identification of the bacterial markers associated with particular inflammatory skin diseases would significantly accelerate the diagnostics and reduce treatment costs. Microbiota research and determination could facilitate the identification of potential causes of skin diseases that cannot be detected by simpler methods, thereby contributing to the design and development of more effective therapies.

Download Full-text

Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class Mammalia

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1801302115 ◽

2018 ◽

Vol 115 (25) ◽

pp. E5786-E5795 ◽

Cited By ~ 59

Author(s):

Ashley A. Ross ◽

Kirsten M. Müller ◽

J. Scott Weese ◽

Josh D. Neufeld

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Human Skin ◽

Microbial Community Composition ◽

Geographic Location ◽

The Body ◽

16S Rrna Genes ◽

Rrna Genes ◽

Skin Microbiome ◽

Skin Microbiota

Skin is the largest organ of the body and represents the primary physical barrier between mammals and their external environment, yet the factors that govern skin microbial community composition among mammals are poorly understood. The objective of this research was to generate a skin microbiota baseline for members of the class Mammalia, testing the effects of host species, geographic location, body region, and biological sex. Skin from the back, torso, and inner thighs of 177 nonhuman mammals was sampled, representing individuals from 38 species and 10 mammalian orders. Animals were sampled from farms, zoos, households, and the wild. The DNA extracts from all skin swabs were amplified by PCR and sequenced, targeting the V3-V4 regions of bacterial and archaeal 16S rRNA genes. Previously published skin microbiome data from 20 human participants, sampled and sequenced using an identical protocol to the nonhuman mammals, were included to make this a comprehensive analysis. Human skin microbial communities were distinct and significantly less diverse than all other sampled mammalian orders. The factor most strongly associated with microbial community data for all samples was whether the host was a human. Within nonhuman samples, host taxonomic order was the most significant factor influencing skin microbiota, followed by the geographic location of the habitat. By comparing the congruence between host phylogeny and microbial community dendrograms, we observed that Artiodactyla (even-toed ungulates) and Perissodactyla (odd-toed ungulates) had significant congruence, providing evidence of phylosymbiosis between skin microbial communities and their hosts.

Download Full-text

Challenges in exploring and manipulating the human skin microbiome

Microbiome ◽

10.1186/s40168-021-01062-5 ◽

2021 ◽

Vol 9 (1) ◽

Author(s):

Manon Boxberger ◽

Valérie Cenizo ◽

Nadim Cassir ◽

Bernard La Scola

Keyword(s):

Human Skin ◽

Human Body ◽

Skin Aging ◽

Microbial Populations ◽

Skin Microbiome ◽

Microbiota Composition ◽

Skin Microbiota ◽

Extrinsic Factors ◽

Health And Disease ◽

Intrinsic And Extrinsic Factors

AbstractThe skin is the exterior interface of the human body with the environment. Despite its harsh physical landscape, the skin is colonized by diverse commensal microbes. In this review, we discuss recent insights into skin microbial populations, including their composition and role in health and disease and their modulation by intrinsic and extrinsic factors, with a focus on the pathobiological basis of skin aging. We also describe the most recent tools for investigating the skin microbiota composition and microbe-skin relationships and perspectives regarding the challenges of skin microbiome manipulation.

Download Full-text

Comprehensive skin microbiome analysis reveals the uniqueness of human-associated microbial communities among the class Mammalia

10.1101/201434 ◽

2017 ◽

Cited By ~ 2

Author(s):

Ashley A. Ross ◽

Kirsten Müller ◽

J. Scott Weese ◽

Josh D. Neufeld

Keyword(s):

Human Skin ◽

External Environment ◽

Geographic Location ◽

The Body ◽

Conservation Strategies ◽

Body Region ◽

Rrna Gene ◽

Skin Microbiome ◽

Skin Microbiota ◽

Mammalian Skin

AbstractSkin is the largest organ of the body and represents the primary physical barrier between mammals and their external environment. The objective of this research was to generate a skin microbiota baseline for members of the class Mammalia, testing the effects of host species, geographic location, body region, and biological sex. The back, torso, and inner thigh regions of 177 non-human mammals were collected to include representatives from 38 species and 10 mammalian orders. Animals were collected from local farms, zoos, households, and the wild. All samples were amplified using the V3-V4 16S rRNA gene region and sequenced using a MiSeq (Illumina). For reference, previously published skin microbiome data from 20 human participants, sampled using an identical protocol to the non-human mammals, were included in the analysis. Human skin was significantly less diverse than all other mammalian orders and the factor most strongly associated with community variation for all samples was whether the host was a human. Within non-human samples, host taxonomic order was the most significant factor influencing the skin community, followed by the geographic location of the habitat. By comparing the congruence between known host phylogeny and microbial community dendrograms, we observed that Artiodactyla (even-toed ungulates) and Perissodactyla (odd-toed ungulates) had significant congruence, providing first evidence of phylosymbiosis between skin communities and their hosts.SignificanceSkin forms a critical protective barrier between a mammal and its external environment. Baseline data on the mammalian skin microbiome is crucial for making informed decisions related to veterinary research and biodiversity conservation strategies, in addition to providing insight into mammalian evolutionary history. To our knowledge, this study represents the largest mammalian skin microbiota project to date. These findings demonstrate that human skin is distinct, not only from other Primates, but from all 10 mammalian orders sampled. Using phylosymbiosis analysis, we provide the first evidence that co-evolution may be occurring between skin communities and their mammalian hosts, which warrants more in-depth future studies of the relationships between mammals and their skin microbiota.

Download Full-text

Temporal Stability of the Human Skin Microbiome

Cell ◽

10.1016/j.cell.2016.04.008 ◽

2016 ◽

Vol 165 (4) ◽

pp. 854-866 ◽

Cited By ~ 318

Author(s):

Julia Oh ◽

Allyson L. Byrd ◽

Morgan Park ◽

Heidi H. Kong ◽

Julia A. Segre

Keyword(s):

Human Skin ◽

Temporal Stability ◽

Skin Microbiome

Download Full-text

Pomegranate Juice and Extract Consumption Increases the Resistance to UVB-induced Erythema and Changes the Skin Microbiome in Healthy Women: a Randomized Controlled Trial

Scientific Reports ◽

10.1038/s41598-019-50926-2 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 3

Author(s):

Susanne M. Henning ◽

Jieping Yang ◽

Ru-Po Lee ◽

Jianjun Huang ◽

Mark Hsu ◽

...

Keyword(s):

Animal Studies ◽

Controlled Trial ◽

Pomegranate Juice ◽

Skin Microbiome ◽

Skin Damage ◽

Skin Microbiota ◽

Open Label ◽

Randomized Controlled ◽

Significant Difference

Abstract In vitro and animal studies have demonstrated that topical application and oral consumption of pomegranate reduces UVB-induced skin damage. We therefore investigated if oral pomegranate consumption will reduce photodamage from UVB irradiation and alter the composition of the skin microbiota in a randomized controlled, parallel, three-arm, open label study. Seventy-four female participants (30–45 years) with Fitzpatrick skin type II-IV were randomly assigned (1:1:1) to 1000 mg of pomegranate extract (PomX), 8 oz of pomegranate juice (PomJ) or placebo for 12 weeks. Minimal erythema dose (MED) and melanin index were determined using a cutometer (mexameter probe). Skin microbiota was determined using 16S rRNA sequencing. The MED was significantly increased in the PomX and PomJ group compared to placebo. There was no significant difference on phylum, but on family and genus level bacterial composition of skin samples collected at baseline and after 12 week intervention showed significant differences between PomJ, PomX and placebo. Members of the Methylobacteriaceae family contain pigments absorbing UV irradiation and might contribute to UVB skin protection. However, we were not able to establish a direct correlation between increased MED and bacterial abundance. In summary daily oral pomegranate consumption may lead to enhanced protection from UV photodamage.

Download Full-text

The Human Skin Microbiome Associates with the Outcome of and Is Influenced by Bacterial Infection

mBio ◽

10.1128/mbio.01315-15 ◽

2015 ◽

Vol 6 (5) ◽

Cited By ~ 54

Author(s):

Julia J. van Rensburg ◽

Huaiying Lin ◽

Xiang Gao ◽

Evelyn Toh ◽

Kate R. Fortney ◽

...

Keyword(s):

Human Skin ◽

Bacterial Species ◽

Haemophilus Ducreyi ◽

16S Rrna Genes ◽

Rrna Genes ◽

Multiple Time ◽

Skin Microbiome ◽

Skin Microbiota ◽

Content Type ◽

Curtis Dissimilarity

ABSTRACTThe influence of the skin microbiota on host susceptibility to infectious agents is largely unexplored. The skin harbors diverse bacterial species that may promote or antagonize the growth of an invading pathogen. We developed a human infection model forHaemophilus ducreyiin which human volunteers are inoculated on the upper arm. After inoculation, papules form and either spontaneously resolve or progress to pustules. To examine the role of the skin microbiota in the outcome ofH. ducreyiinfection, we analyzed the microbiomes of four dose-matched pairs of “resolvers” and “pustule formers” whose inoculation sites were swabbed at multiple time points. Bacteria present on the skin were identified by amplification and pyrosequencing of 16S rRNA genes. Nonmetric multidimensional scaling (NMDS) using Bray-Curtis dissimilarity between the preinfection microbiomes of infected sites showed that sites from the same volunteer clustered together and that pustule formers segregated from resolvers (P= 0.001, permutational multivariate analysis of variance [PERMANOVA]), suggesting that the preinfection microbiomes were associated with outcome. NMDS using Bray-Curtis dissimilarity of the endpoint samples showed that the pustule sites clustered together and were significantly different than the resolved sites (P= 0.001, PERMANOVA), suggesting that the microbiomes at the endpoint differed between the two groups. In addition toH. ducreyi, pustule-forming sites had a greater abundance ofProteobacteria,Bacteroidetes,Micrococcus,Corynebacterium,Paracoccus, andStaphylococcusspecies, whereas resolved sites had higher levels ofActinobacteriaandPropionibacteriumspecies. These results suggest that at baseline, resolvers and pustule formers have distinct skin bacterial communities which change in response to infection and the resultant immune response.IMPORTANCEHuman skin is home to a diverse community of microorganisms, collectively known as the skin microbiome. Some resident bacteria are thought to protect the skin from infection by outcompeting pathogens for resources or by priming the immune system's response to invaders. However, the influence of the skin microbiome on the susceptibility to or protection from infection has not been prospectively evaluated in humans. We characterized the skin microbiome before, during, and after experimental inoculation of the arm withHaemophilus ducreyiin matched volunteers who subsequently resolved the infection or formed abscesses. Our results suggest that the preinfection microbiomes of pustule formers and resolvers have distinct community structures which change in response to the progression ofH. ducreyiinfection to abscess formation.

Download Full-text

Cutibacterium acnes (Propionibacterium acnes) 16S rRNA Genotyping of Microbial Samples from Possessions Contributes to Owner Identification

mSystems ◽

10.1128/msystems.00594-19 ◽

2019 ◽

Vol 4 (6) ◽

Cited By ~ 3

Author(s):

Jiayue Yang ◽

Tomoya Tsukimi ◽

Mia Yoshikawa ◽

Kenta Suzuki ◽

Tomoki Takeda ◽

...

Keyword(s):

16S Rrna ◽

Human Skin ◽

Rrna Gene ◽

Skin Microbiome ◽

Nucleotide Polymorphisms ◽

Skin Microbiota ◽

Content Type ◽

Microbiome Profile ◽

Cutibacterium Acnes ◽

Genotype Composition

ABSTRACT The human skin surface harbors huge numbers of microbes. The skin microbiota interacts with its host and forms a skin microbiome profile that is specific for each individual. It has been reported that the skin microbiota that is left on an individual’s possessions can act as a sort of “fingerprint” and be used for owner identification. However, this approach needs to be improved to take into account any long-term instability of skin microbiota and contamination from nonspecific bacteria. Here, we took advantage of single-nucleotide polymorphisms (SNPs) in the 16S-encoding rRNA gene of Cutibacterium acnes, the most common and abundant bacterium on human skin, to perform owner identification. We first developed a high-throughput genotyping method based on next-generation sequencing to characterize the SNPs of the C. acnes 16S rRNA gene and found that the genotype composition of C. acnes 16S rRNA is individual specific. Owner identification accuracy of around 90% based on random forest machine learning was achieved by using a combination of C. acnes 16S rRNA genotype and skin microbiome profile data. Furthermore, our study showed that the C. acnes 16S rRNA genotype remained more stable over time than the skin microbiome profile. This characteristic of C. acnes was further confirmed by the analysis of publicly available human skin metagenome data. Our approach, with its high precision, good reproducibility, and low costs, thus provides new possibilities in the field of microbiome-based owner identification and forensics in general. IMPORTANCE Cutibacterium acnes is the most common and abundant bacterial species on human skin, and the gene that encodes its 16S rRNA has multiple single-nucleotide polymorphisms. In this study, we developed a method to efficiently determine the C. acnes 16S rRNA genotype composition from microbial samples taken from the hands of participants and from their possessions. Using the C. acnes 16S rRNA genotype composition, we could predict the owner of a possession with around 90% accuracy when the 16S rRNA gene-based microbiome profile was included. We also showed that the C. acnes 16S rRNA genotype composition was more stable over time than the skin microbiome profile and thus is more suitable for owner identification.

Download Full-text