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Anatomy promotes neutral coexistence of strains in the human skin microbiome.

ABSTRACT: What enables strains of the same species to coexist in a microbiome? Here, we investigate whether host anatomy can explain strain co-residence of Cutibacterium acnes, the most abundant species on human skin. We reconstruct on-person evolution and migration using whole-genome sequencing of C. acnes colonies acquired from healthy subjects, including from individual skin pores, and find considerable spatial structure at the level of pores. Although lineages (sets of colonies separated by <100 mutations) with in vitro fitness differences coexist within centimeter-scale regions, each pore is dominated by a single lineage. Moreover, colonies from a pore typically have identical genomes. An absence of adaptive signatures suggests a genotype-independent source of low within-pore diversity. We therefore propose that pore anatomy imposes random single-cell bottlenecks; the resulting population fragmentation reduces competition and promotes coexistence. Our findings suggest that therapeutic interventions involving pore-dwelling species might focus on removing resident populations over optimizing probiotic fitness.

SUBMITTER: Conwill A

PROVIDER: S-EPMC8831475 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Anatomy promotes neutral coexistence of strains in the human skin microbiome.

Conwill Arolyn A Kuan Anne C AC Damerla Ravalika R Poret Alexandra J AJ Baker Jacob S JS Tripp A Delphine AD Alm Eric J EJ Lieberman Tami D TD

Cell host & microbe 20220106 2

What enables strains of the same species to coexist in a microbiome? Here, we investigate whether host anatomy can explain strain co-residence of Cutibacterium acnes, the most abundant species on human skin. We reconstruct on-person evolution and migration using whole-genome sequencing of C. acnes colonies acquired from healthy subjects, including from individual skin pores, and find considerable spatial structure at the level of pores. Although lineages (sets of colonies separated by <100 mutat ...[more]

PMID: 34995483

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Project description:Human skin microbiota has been described as a "microbial fingerprint" due to observed differences between individuals. Current understanding of the cutaneous microbiota is based on sampling the outermost layers of the epidermis, while the microbiota in the remaining skin layers has not yet been fully characterized. Environmental conditions can vary drastically between the cutaneous compartments and give rise to unique communities. We demonstrate that the dermal microbiota is surprisingly similar among individuals and contains a specific subset of the epidermal microbiota. Variability in bacterial community composition decreased significantly from the epidermal to the dermal compartment but was similar among anatomic locations (hip and knee). The composition of the epidermal microbiota was more strongly affected by environmental factors than that of the dermal community. These results indicate a well-conserved dermal community that is functionally distinct from the epidermal community, challenging the current dogma. Future studies in cutaneous disorders and chronic infections may benefit by focusing on the dermal microbiota as a persistent microbial community.IMPORTANCE Human skin microbiota is thought to be unique according to the individual's lifestyle and genetic predisposition. This is true for the epidermal microbiota, while our findings demonstrate that the dermal microbiota is universal between healthy individuals. The preserved dermal microbial community is compositionally unique and functionally distinct to the specific environment in the depth of human skin. It is expected to have direct contact with the immune response of the human host, and research in the communication between host and microbiota should be targeted to this cutaneous compartment. This novel insight into specific microbial adaptation can be used advantageously in the research of chronic disorders and infections of the skin. It can enlighten the alteration between health and disease to the benefit of patients suffering from long-lasting socioeconomic illnesses.

Project description:BackgroundThe past decade of microbiome research has concentrated on cataloging the diversity of taxa in different environments. The next decade is poised to focus on microbial traits and function. Most existing methods for doing this perform pathway analysis using reference databases. This has both benefits and drawbacks. Function can go undetected if reference databases are coarse-grained or incomplete. Likewise, detection of a pathway does not guarantee expression of the associated function. Finally, function cannot be connected to specific microbial constituents, making it difficult to ascertain the types of organisms exhibiting particular traits-something that is important for understanding microbial success in specific environments. A complementary approach to pathway analysis is to use the wealth of microbial trait information collected over years of lab-based, culture experiments.MethodsHere, we use journal articles and Bergey's Manual of Systematic Bacteriology to develop a trait-based database for 971 human skin bacterial taxa. We then use this database to examine functional traits that are over/underrepresented among skin taxa. Specifically, we focus on three trait classes-binary, categorical, and quantitative-and compare trait values among skin taxa and microbial taxa more broadly. We compare binary traits using a Chi-square test, categorical traits using randomization trials, and quantitative traits using a nonparametric relative effects test based on global rankings using Tukey contrasts.ResultsWe find a number of traits that are over/underrepresented within the human skin microbiome. For example, spore formation, acid phosphatase, alkaline phosphatase, pigment production, catalase, and oxidase are all less common among skin taxa. As well, skin bacteria are less likely to be aerobic, favoring, instead, a facultative strategy. They are also less likely to exhibit gliding motility, less likely to be spirillum or rod-shaped, and less likely to grow in chains. Finally, skin bacteria have more difficulty at high pH, prefer warmer temperatures, and are much less resilient to hypotonic conditions.ConclusionsOur analysis shows how an approach that relies on information from culture experiments can both support findings from pathway analysis, and also generate new insights into the structuring principles of microbial communities.

Dataset Information

Anatomy promotes neutral coexistence of strains in the human skin microbiome.

Publications

Anatomy promotes neutral coexistence of strains in the human skin microbiome.

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