Zhiming Li1,2, Jingjing Xia3,4,5, Liuyiqi Jiang3, Yimei Tan4,6, Yitai An1,2, Xingyu Zhu4,7, Jie Ruan1,2, Zhihua Chen1,2, Hefu Zhen1,2, Yanyun Ma4,7, Zhuye Jie1,2, Liang Xiao1,2, Huanming Yang1,2, Jian Wang1,2, Karsten Kristiansen1,2,8, Xun Xu1,2,9, Li Jin4,10, Chao Nie11,12, Jean Krutmann13,14,15, Xiao Liu16,17,18, Jiucun Wang19,20,21,22. 1. BGI-Shenzhen, Shenzhen, China. 2. China National Genebank, Shenzhen, China. 3. State Key Laboratory of Genetic Engineering, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, and Department of Dermatology, Huashan Hospital, Fudan University, Shanghai, China. 4. Human Phenome Institute, Fudan University, Shanghai, China. 5. IUF-Leibniz Research Institute for Environmental Medicine, Düsseldorf, Germany. 6. Department of Skin & Cosmetic Research, Shanghai Skin Disease Hospital, Shanghai, China. 7. Institute for Six-sector Economy, Fudan University, Shanghai, China. 8. Laboratory of Genomics and Molecular Biomedicine, Department of Biology, University of Copenhagen, Copenhagen, Denmark. 9. Guangdong Provincial Key Laboratory of Genome Read and Write, Shenzhen, China. 10. Research Unit of Dissecting the Population Genetics and Developing New Technologies for Treatment and Prevention of Dermatological Diseases (2019RU058), Chinese Academy of Medical Sciences, Shanghai, China. 11. BGI-Shenzhen, Shenzhen, China. niechao@genomics.cn. 12. China National Genebank, Shenzhen, China. niechao@genomics.cn. 13. Human Phenome Institute, Fudan University, Shanghai, China. Jean.Krutmann@iuf-duesseldorf.de. 14. IUF-Leibniz Research Institute for Environmental Medicine, Düsseldorf, Germany. Jean.Krutmann@iuf-duesseldorf.de. 15. Medical Faculty, Heinrich-Heine University, Düsseldorf, Germany. Jean.Krutmann@iuf-duesseldorf.de. 16. BGI-Shenzhen, Shenzhen, China. liuxiao@sz.tsinghua.edu.cn. 17. Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, China. liuxiao@sz.tsinghua.edu.cn. 18. BGI Education Center, University of Chinese Academy of Sciences, Shenzhen, China. liuxiao@sz.tsinghua.edu.cn. 19. State Key Laboratory of Genetic Engineering, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, and Department of Dermatology, Huashan Hospital, Fudan University, Shanghai, China. jcwang@fudan.edu.cn. 20. Human Phenome Institute, Fudan University, Shanghai, China. jcwang@fudan.edu.cn. 21. Research Unit of Dissecting the Population Genetics and Developing New Technologies for Treatment and Prevention of Dermatological Diseases (2019RU058), Chinese Academy of Medical Sciences, Shanghai, China. jcwang@fudan.edu.cn. 22. Institute of Rheumatology, Immunology and Allergy, Fudan University, Shanghai, China. jcwang@fudan.edu.cn.
Abstract
BACKGROUND: The human skin microbiota is considered to be essential for skin homeostasis and barrier function. Comprehensive analyses of its function would substantially benefit from a catalog of reference genes derived from metagenomic sequencing. The existing catalog for the human skin microbiome is based on samples from limited individuals from a single cohort on reference genomes, which limits the coverage of global skin microbiome diversity. RESULTS: In the present study, we have used shotgun metagenomics to newly sequence 822 skin samples from Han Chinese, which were subsequently combined with 538 previously sequenced North American samples to construct an integrated Human Skin Microbial Gene Catalog (iHSMGC). The iHSMGC comprised 10,930,638 genes with the detection of 4,879,024 new genes. Characterization of the human skin resistome based on iHSMGC confirmed that skin commensals, such as Staphylococcus spp, are an important reservoir of antibiotic resistance genes (ARGs). Further analyses of skin microbial ARGs detected microbe-specific and skin site-specific ARG signatures. Of note, the abundance of ARGs was significantly higher in Chinese than Americans, while multidrug-resistant bacteria ("superbugs") existed on the skin of both Americans and Chinese. A detailed analysis of microbial signatures identified Moraxella osloensis as a species specific for Chinese skin. Importantly, Moraxella osloensis proved to be a signature species for one of two robust patterns of microbial networks present on Chinese skin, with Cutibacterium acnes indicating the second one. Each of such "cutotypes" was associated with distinct patterns of data-driven marker genes, functional modules, and host skin properties. The two cutotypes markedly differed in functional modules related to their metabolic characteristics, indicating that host-dependent trophic chains might underlie their development. CONCLUSIONS: The development of the iHSMGC will facilitate further studies on the human skin microbiome. In the present study, it was used to further characterize the human skin resistome. It also allowed to discover the existence of two cutotypes on the human skin. The latter finding will contribute to a better understanding of the interpersonal complexity of the skin microbiome. Video abstract.
BACKGROUND: The human skin microbiota is considered to be essential for skin homeostasis and barrier function. Comprehensive analyses of its function would substantially benefit from a catalog of reference genes derived from metagenomic sequencing. The existing catalog for the human skin microbiome is based on samples from limited individuals from a single cohort on reference genomes, which limits the coverage of global skin microbiome diversity. RESULTS: In the present study, we have used shotgun metagenomics to newly sequence 822 skin samples from Han Chinese, which were subsequently combined with 538 previously sequenced North American samples to construct an integrated Human Skin Microbial Gene Catalog (iHSMGC). The iHSMGC comprised 10,930,638 genes with the detection of 4,879,024 new genes. Characterization of the human skin resistome based on iHSMGC confirmed that skin commensals, such as Staphylococcus spp, are an important reservoir of antibiotic resistance genes (ARGs). Further analyses of skin microbial ARGs detected microbe-specific and skin site-specific ARG signatures. Of note, the abundance of ARGs was significantly higher in Chinese than Americans, while multidrug-resistant bacteria ("superbugs") existed on the skin of both Americans and Chinese. A detailed analysis of microbial signatures identified Moraxella osloensis as a species specific for Chinese skin. Importantly, Moraxella osloensis proved to be a signature species for one of two robust patterns of microbial networks present on Chinese skin, with Cutibacterium acnes indicating the second one. Each of such "cutotypes" was associated with distinct patterns of data-driven marker genes, functional modules, and host skin properties. The two cutotypes markedly differed in functional modules related to their metabolic characteristics, indicating that host-dependent trophic chains might underlie their development. CONCLUSIONS: The development of the iHSMGC will facilitate further studies on the human skin microbiome. In the present study, it was used to further characterize the human skin resistome. It also allowed to discover the existence of two cutotypes on the human skin. The latter finding will contribute to a better understanding of the interpersonal complexity of the skin microbiome. Video abstract.
Authors: Rob Knight; Alison Vrbanac; Bryn C Taylor; Alexander Aksenov; Chris Callewaert; Justine Debelius; Antonio Gonzalez; Tomasz Kosciolek; Laura-Isobel McCall; Daniel McDonald; Alexey V Melnik; James T Morton; Jose Navas; Robert A Quinn; Jon G Sanders; Austin D Swafford; Luke R Thompson; Anupriya Tripathi; Zhenjiang Z Xu; Jesse R Zaneveld; Qiyun Zhu; J Gregory Caporaso; Pieter C Dorrestein Journal: Nat Rev Microbiol Date: 2018-07 Impact factor: 60.633
Authors: Nanna Fyhrquist; Gareth Muirhead; Stefanie Prast-Nielsen; Marine Jeanmougin; Peter Olah; Tiina Skoog; Gerome Jules-Clement; Micha Feld; Mauricio Barrientos-Somarribas; Hanna Sinkko; Ellen H van den Bogaard; Patrick L J M Zeeuwen; Gijs Rikken; Joost Schalkwijk; Hanna Niehues; Walter Däubener; Silvia Kathrin Eller; Helen Alexander; Davide Pennino; Sari Suomela; Ioannis Tessas; Emilia Lybeck; Anna M Baran; Hamid Darban; Roopesh Singh Gangwar; Ulrich Gerstel; Katharina Jahn; Piia Karisola; Lee Yan; Britta Hansmann; Shintaro Katayama; Stephan Meller; Max Bylesjö; Philippe Hupé; Francesca Levi-Schaffer; Dario Greco; Annamari Ranki; Jens M Schröder; Jonathan Barker; Juha Kere; Sophia Tsoka; Antti Lauerma; Vassili Soumelis; Frank O Nestle; Bernhard Homey; Björn Andersson; Harri Alenius Journal: Nat Commun Date: 2019-10-16 Impact factor: 14.919
Authors: Bing Ma; Michael T France; Jonathan Crabtree; Johanna B Holm; Michael S Humphrys; Rebecca M Brotman; Jacques Ravel Journal: Nat Commun Date: 2020-02-26 Impact factor: 14.919