The Phageome in Normal and Inflamed Human Skin

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2023 Sep 29

PMID 37774017

Authors

M Wielscher

K Pfisterer

D Samardzic

P Balsini

C Bangert

K Jager

M Buchberger

B Selitsch

P Pjevac

B Willinger

W Weninger

Affiliations

Soon will be listed here.

Abstract

Dysbiosis of skin microbiota drives the progression of atopic dermatitis (AD). The contribution of bacteriophages to bacterial community compositions in normal and inflamed skin is unknown. Using shotgun metagenomics from skin swabs of healthy individuals and patients with AD, we found 13,586 potential viral contiguous DNA sequences, which could be combined into 164 putative viral genomes including 133 putative phages. The Shannon diversity index for the viral metagenome-assembled genomes (vMAGs) did not correlate with AD. In total, we identified 28 vMAGs that differed significantly between normal and AD skin. Quantitative polymerase chain reaction validation of three complete vMAGs revealed their independence from host bacterium abundance. Our data indicate that normal and inflamed skin harbor distinct phageomes and suggest a causative relationship between changing viral and bacterial communities as a driver of skin pathology.

Citing Articles

Prophages in : Distribution and genetic diversity.

Gaibani P, Latorre R Heliyon. 2025; 11(4):e42755.

PMID: 40066052 PMC: 11891724. DOI: 10.1016/j.heliyon.2025.e42755.

Cutibacterium acnes bacteriophage therapy: exploring a new frontier in acne vulgaris treatment.

Mohammadi M Arch Dermatol Res. 2024; 317(1):84.

PMID: 39644414 DOI: 10.1007/s00403-024-03585-x.

Bacteriophages from human skin infecting coagulase-negative Staphylococcus: diversity, novelty and host resistance.

Alsaadi S, Lu H, Zhang M, Dykes G, Allison H, Horsburgh M Sci Rep. 2024; 14(1):8245.

PMID: 38589670 PMC: 11001980. DOI: 10.1038/s41598-024-59065-9.

References

Cantalapiedra C, Hernandez-Plaza A, Letunic I, Bork P, Huerta-Cepas J . eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Mol Biol Evol. 2021; 38(12):5825-5829. PMC: 8662613. DOI: 10.1093/molbev/msab293. View

Shaffer M, Borton M, McGivern B, Zayed A, La Rosa S, Solden L . DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 2020; 48(16):8883-8900. PMC: 7498326. DOI: 10.1093/nar/gkaa621. View

Ecale Zhou C, Kimbrel J, Edwards R, McNair K, Souza B, Malfatti S . MultiPhATE2: code for functional annotation and comparison of phage genomes. G3 (Bethesda). 2021; 11(5). PMC: 8104953. DOI: 10.1093/g3journal/jkab074. View

Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar G, Sonnhammer E . Pfam: The protein families database in 2021. Nucleic Acids Res. 2020; 49(D1):D412-D419. PMC: 7779014. DOI: 10.1093/nar/gkaa913. View

Hyatt D, Chen G, LoCascio P, Land M, Larimer F, Hauser L . Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010; 11:119. PMC: 2848648. DOI: 10.1186/1471-2105-11-119. View

Uritskiy G, DiRuggiero J, Taylor J . MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome. 2018; 6(1):158. PMC: 6138922. DOI: 10.1186/s40168-018-0541-1. View

Hevroni G, Flores-Uribe J, Beja O, Philosof A . Seasonal and diel patterns of abundance and activity of viruses in the Red Sea. Proc Natl Acad Sci U S A. 2020; 117(47):29738-29747. PMC: 7703586. DOI: 10.1073/pnas.2010783117. View

Wang L, Zhang G, Xu H, Xin H, Zhang Y . Metagenomic Analyses of Microbial and Carbohydrate-Active Enzymes in the Rumen of Holstein Cows Fed Different Forage-to-Concentrate Ratios. Front Microbiol. 2019; 10:649. PMC: 6449447. DOI: 10.3389/fmicb.2019.00649. View

Little J, Dedrick R, Freeman K, Cristinziano M, Smith B, Benson C . Bacteriophage treatment of disseminated cutaneous Mycobacterium chelonae infection. Nat Commun. 2022; 13(1):2313. PMC: 9064978. DOI: 10.1038/s41467-022-29689-4. View

10.

Soding J . Protein homology detection by HMM-HMM comparison. Bioinformatics. 2004; 21(7):951-60. DOI: 10.1093/bioinformatics/bti125. View

11.

Faruque S, Islam M, Ahmad Q, Faruque A, Sack D, Nair G . Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage. Proc Natl Acad Sci U S A. 2005; 102(17):6119-24. PMC: 1087956. DOI: 10.1073/pnas.0502069102. View

12.

Kang D, Li F, Kirton E, Thomas A, Egan R, An H . MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019; 7:e7359. PMC: 6662567. DOI: 10.7717/peerj.7359. View

13.

Byrd A, Belkaid Y, Segre J . The human skin microbiome. Nat Rev Microbiol. 2018; 16(3):143-155. DOI: 10.1038/nrmicro.2017.157. View

14.

Nobrega F, Vlot M, de Jonge P, Dreesens L, Beaumont H, Lavigne R . Targeting mechanisms of tailed bacteriophages. Nat Rev Microbiol. 2018; 16(12):760-773. DOI: 10.1038/s41579-018-0070-8. View

15.

Roux S, Paez-Espino D, Chen I, Palaniappan K, Ratner A, Chu K . IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses. Nucleic Acids Res. 2020; 49(D1):D764-D775. PMC: 7778971. DOI: 10.1093/nar/gkaa946. View

16.

Knowles B, Silveira C, Bailey B, Barott K, Cantu V, Cobian-Guemes A . Lytic to temperate switching of viral communities. Nature. 2016; 531(7595):466-70. DOI: 10.1038/nature17193. View

17.

Saheb Kashaf S, Almeida A, Segre J, Finn R . Recovering prokaryotic genomes from host-associated, short-read shotgun metagenomic sequencing data. Nat Protoc. 2021; 16(5):2520-2541. DOI: 10.1038/s41596-021-00508-2. View

18.

Hanifin J, Rogge J . Staphylococcal infections in patients with atopic dermatitis. Arch Dermatol. 1977; 113(10):1383-6. View

19.

Brunello L . Atopic dermatitis. Nat Rev Dis Primers. 2018; 4(1):2. DOI: 10.1038/s41572-018-0004-9. View

20.

Seed K, Lazinski D, Calderwood S, Camilli A . A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature. 2013; 494(7438):489-91. PMC: 3587790. DOI: 10.1038/nature11927. View