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      Cutaneous Malassezia: Commensal, Pathogen, or Protector?

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          Abstract

          The skin microbial community is a multifunctional ecosystem aiding prevention of infections from transient pathogens, maintenance of host immune homeostasis, and skin health. A better understanding of the complex milieu of microbe-microbe and host-microbe interactions will be required to define the ecosystem’s optimal function and enable rational design of microbiome targeted interventions. Malassezia, a fungal genus currently comprising 18 species and numerous functionally distinct strains, are lipid-dependent basidiomycetous yeasts and integral components of the skin microbiome. The high proportion of Malassezia in the skin microbiome makes understanding their role in healthy and diseased skin crucial to development of functional skin health knowledge and understanding of normal, healthy skin homeostasis. Over the last decade, new tools for Malassezia culture, detection, and genetic manipulation have revealed not only the ubiquity of Malassezia on skin but new pathogenic roles in seborrheic dermatitis, psoriasis, Crohn’s disease, and pancreatic ductal carcinoma. Application of these tools continues to peel back the layers of Malassezia/skin interactions, including clear examples of pathogenicity, commensalism, and potential protective or beneficial activities creating mutualism. Our increased understanding of host- and microbe-specific interactions should lead to identification of key factors that maintain skin in a state of healthy mutualism or, in turn, initiate pathogenic changes. These approaches are leading toward development of new therapeutic targets and treatment options. This review discusses recent developments that have expanded our understanding of Malassezia’s role in the skin microbiome, with a focus on its multiple roles in health and disease as commensal, pathogen, and protector.

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          Most cited references221

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          Enterotypes of the human gut microbiome.

          Our knowledge of species and functional composition of the human gut microbiome is rapidly increasing, but it is still based on very few cohorts and little is known about variation across the world. By combining 22 newly sequenced faecal metagenomes of individuals from four countries with previously published data sets, here we identify three robust clusters (referred to as enterotypes hereafter) that are not nation or continent specific. We also confirmed the enterotypes in two published, larger cohorts, indicating that intestinal microbiota variation is generally stratified, not continuous. This indicates further the existence of a limited number of well-balanced host-microbial symbiotic states that might respond differently to diet and drug intake. The enterotypes are mostly driven by species composition, but abundant molecular functions are not necessarily provided by abundant species, highlighting the importance of a functional analysis to understand microbial communities. Although individual host properties such as body mass index, age, or gender cannot explain the observed enterotypes, data-driven marker genes or functional modules can be identified for each of these host properties. For example, twelve genes significantly correlate with age and three functional modules with the body mass index, hinting at a diagnostic potential of microbial markers.
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            Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.

            Upon delivery, the neonate is exposed for the first time to a wide array of microbes from a variety of sources, including maternal bacteria. Although prior studies have suggested that delivery mode shapes the microbiota's establishment and, subsequently, its role in child health, most researchers have focused on specific bacterial taxa or on a single body habitat, the gut. Thus, the initiation stage of human microbiome development remains obscure. The goal of the present study was to obtain a community-wide perspective on the influence of delivery mode and body habitat on the neonate's first microbiota. We used multiplexed 16S rRNA gene pyrosequencing to characterize bacterial communities from mothers and their newborn babies, four born vaginally and six born via Cesarean section. Mothers' skin, oral mucosa, and vagina were sampled 1 h before delivery, and neonates' skin, oral mucosa, and nasopharyngeal aspirate were sampled <5 min, and meconium <24 h, after delivery. We found that in direct contrast to the highly differentiated communities of their mothers, neonates harbored bacterial communities that were undifferentiated across multiple body habitats, regardless of delivery mode. Our results also show that vaginally delivered infants acquired bacterial communities resembling their own mother's vaginal microbiota, dominated by Lactobacillus, Prevotella, or Sneathia spp., and C-section infants harbored bacterial communities similar to those found on the skin surface, dominated by Staphylococcus, Corynebacterium, and Propionibacterium spp. These findings establish an important baseline for studies tracking the human microbiome's successional development in different body habitats following different delivery modes, and their associated effects on infant health.
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              The human skin microbiome

              Functioning as the exterior interface of the human body with the environment, skin acts as a physical barrier to prevent the invasion of foreign pathogens while providing a home to the commensal microbiota. The harsh physical landscape of skin, particularly the desiccated, nutrient-poor, acidic environment, also contributes to the adversity that pathogens face when colonizing human skin. Despite this, the skin is colonized by a diverse microbiota. In this Review, we describe amplicon and shotgun metagenomic DNA sequencing studies that have been used to assess the taxonomic diversity of microorganisms that are associated with skin from the kingdom to the strain level. We discuss recent insights into skin microbial communities, including their composition in health and disease, the dynamics between species and interactions with the immune system, with a focus on Propionibacterium acnes, Staphylococcus epidermidis and Staphylococcus aureus.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/1144056
                URI : https://loop.frontiersin.org/people/1144020
                URI : https://loop.frontiersin.org/people/739924
                URI : https://loop.frontiersin.org/people/916196
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                26 January 2021
                2020
                : 10
                : 614446
                Affiliations
                [1] 1 Skin Research Institute of Singapore, Agency for Science, Technology and Research , Singapore, Singapore
                [2] 2 Department of Drug Discovery, College of Pharmacy, Medical University of South Carolina , Charleston, SC, United States
                Author notes

                Edited by: Guilhem Janbon, Institut Pasteur, France

                Reviewed by: Chaoyang Xue, Rutgers University, Newark, United States; Vishukumar Aimanianda, Institut Pasteur, France

                *Correspondence: John E. Common, john.common@ 123456sris.a-star.edu.sg ; Thomas L. Dawson Jr., thomas_dawson@ 123456sris.a-star.edu.sg

                This article was submitted to Fungal Pathogenesis, a section of the journal Frontiers in Cellular and Infection Microbiology

                †These authors have contributed equally to this work

                Article
                10.3389/fcimb.2020.614446
                7870721
                33575223
                9a5d24d4-4a2f-4e4a-bbd7-5ea45bff3592
                Copyright © 2021 Vijaya Chandra, Srinivas, Dawson and Common

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 06 October 2020
                : 04 December 2020
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 221, Pages: 16, Words: 8154
                Funding
                Funded by: Agency for Science, Technology and Research 10.13039/501100001348
                Award ID: H18/01a0/016, H17/01/a0/004
                Categories
                Cellular and Infection Microbiology
                Review

                Infectious disease & Microbiology
                malassezia,commensal,pathogen,mutualist,multikingdom,immunity,skin,host and disease

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