Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis

IntroductionAtopic dermatitis (AD) is one of the most common inflammatory skin diseases. Skin microecological imbalance is an important factor in the pathogenesis of AD, but the underlying mechanism of its interaction with humans remains unclear.Methods16S rRNA gene sequencing was conducted to revea...

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Main Authors: Kaikai Huang, Fang Li, Yingyao Liu, Baoying Liang, Pinghua Qu, Linlin Yang, Shanshan Han, Wenjun Li, Xiumei Mo, Lei Dong, Ying Lin
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1349674/full
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author Kaikai Huang
Fang Li
Yingyao Liu
Baoying Liang
Pinghua Qu
Linlin Yang
Shanshan Han
Wenjun Li
Xiumei Mo
Xiumei Mo
Xiumei Mo
Lei Dong
Ying Lin
Ying Lin
Ying Lin
author_facet Kaikai Huang
Fang Li
Yingyao Liu
Baoying Liang
Pinghua Qu
Linlin Yang
Shanshan Han
Wenjun Li
Xiumei Mo
Xiumei Mo
Xiumei Mo
Lei Dong
Ying Lin
Ying Lin
Ying Lin
author_sort Kaikai Huang
collection DOAJ
description IntroductionAtopic dermatitis (AD) is one of the most common inflammatory skin diseases. Skin microecological imbalance is an important factor in the pathogenesis of AD, but the underlying mechanism of its interaction with humans remains unclear.Methods16S rRNA gene sequencing was conducted to reveal the skin microbiota dynamics. Changes in skin metabolites were tracked by LC–MS metabolomics. We then explored the potential mechanism of interaction by analyzing the correlation between skin bacterial communities and metabolites in corresponding skin-associated samples.ResultsSamples from 18 AD patients and 18 healthy volunteers (HVs) were subjected to 16S rRNA gene sequencing and LC–MS metabolomics. AD patients had dysbiosis of the skin bacterial community with decreased species richness and evenness. The relative abundance of the genus Staphylococcus increased significantly in AD, while the abundances of the genera Propionibacterium and Brevundimonas decreased significantly. The relative abundance of the genera Staphylococcus in healthy females was significantly higher than those in healthy males, while it showed no difference in AD patients with or without lesions. The effects of AD status, sex and the presence or absence of rashes on the number of differentially abundant metabolites per capita were successively reduced. Multiple metabolites involved in purine metabolism and phenylalanine metabolism pathways (such as xanthosine/xanthine and L-phenylalanine/trans-cinnamate) were increased in AD patients. These trends were much more obvious between female AD patients and female HVs. Spearman correlation analysis revealed that the genus Staphylococcus was positively correlated with various compounds involved in phenylalanine metabolism and purine metabolic pathways. The genera Brevundimonas and Lactobacillus were negatively correlated with various compounds involved in purine metabolism, phenylalanine metabolism and sphingolipid signaling pathways.DiscussionWe suggest that purine metabolism and phenylalanine metabolism pathway disorders may play a certain role in the pathogenic mechanism of Staphylococcus aureus in AD. We also found that females are more likely to be colonized by the genus Staphylococcus than males. Differentially abundant metabolites involved in purine metabolism and phenylalanine metabolism pathways were more obvious in female. However, we should notice that the metabolites we detected do not necessarily derived from microbes, they may also origin from the host.
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spelling doaj.art-19e463afed8a4c619bb1e601fa5088bd2024-03-15T04:54:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-03-011510.3389/fmicb.2024.13496741349674Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitisKaikai Huang0Fang Li1Yingyao Liu2Baoying Liang3Pinghua Qu4Linlin Yang5Shanshan Han6Wenjun Li7Xiumei Mo8Xiumei Mo9Xiumei Mo10Lei Dong11Ying Lin12Ying Lin13Ying Lin14Department of Dermatology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, Guangzhou, ChinaDepartment of Dermatology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaDepartment of Clinical Laboratory, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaDepartment of Dermatology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaDepartment of Dermatology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaDepartment of Dermatology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaState Key Laboratory of Dampness Syndrome of Chinese Medicine, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaGuangdong Provincial Clinical Research Center for Chinese Medicine Dermatology, Guangzhou, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaDepartment of Dermatology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, ChinaGuangdong Provincial Clinical Research Center for Chinese Medicine Dermatology, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Chinese Medicine for Prevention and Treatment of Refractory Chronic Diseases, Guangzhou, ChinaIntroductionAtopic dermatitis (AD) is one of the most common inflammatory skin diseases. Skin microecological imbalance is an important factor in the pathogenesis of AD, but the underlying mechanism of its interaction with humans remains unclear.Methods16S rRNA gene sequencing was conducted to reveal the skin microbiota dynamics. Changes in skin metabolites were tracked by LC–MS metabolomics. We then explored the potential mechanism of interaction by analyzing the correlation between skin bacterial communities and metabolites in corresponding skin-associated samples.ResultsSamples from 18 AD patients and 18 healthy volunteers (HVs) were subjected to 16S rRNA gene sequencing and LC–MS metabolomics. AD patients had dysbiosis of the skin bacterial community with decreased species richness and evenness. The relative abundance of the genus Staphylococcus increased significantly in AD, while the abundances of the genera Propionibacterium and Brevundimonas decreased significantly. The relative abundance of the genera Staphylococcus in healthy females was significantly higher than those in healthy males, while it showed no difference in AD patients with or without lesions. The effects of AD status, sex and the presence or absence of rashes on the number of differentially abundant metabolites per capita were successively reduced. Multiple metabolites involved in purine metabolism and phenylalanine metabolism pathways (such as xanthosine/xanthine and L-phenylalanine/trans-cinnamate) were increased in AD patients. These trends were much more obvious between female AD patients and female HVs. Spearman correlation analysis revealed that the genus Staphylococcus was positively correlated with various compounds involved in phenylalanine metabolism and purine metabolic pathways. The genera Brevundimonas and Lactobacillus were negatively correlated with various compounds involved in purine metabolism, phenylalanine metabolism and sphingolipid signaling pathways.DiscussionWe suggest that purine metabolism and phenylalanine metabolism pathway disorders may play a certain role in the pathogenic mechanism of Staphylococcus aureus in AD. We also found that females are more likely to be colonized by the genus Staphylococcus than males. Differentially abundant metabolites involved in purine metabolism and phenylalanine metabolism pathways were more obvious in female. However, we should notice that the metabolites we detected do not necessarily derived from microbes, they may also origin from the host.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1349674/fullatopic dermatitisskin microbiomeskin metabolomecorrelation analysispurine metabolismphenylalanine metabolism
spellingShingle Kaikai Huang
Fang Li
Yingyao Liu
Baoying Liang
Pinghua Qu
Linlin Yang
Shanshan Han
Wenjun Li
Xiumei Mo
Xiumei Mo
Xiumei Mo
Lei Dong
Ying Lin
Ying Lin
Ying Lin
Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
Frontiers in Microbiology
atopic dermatitis
skin microbiome
skin metabolome
correlation analysis
purine metabolism
phenylalanine metabolism
title Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
title_full Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
title_fullStr Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
title_full_unstemmed Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
title_short Multi-omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
title_sort multi omics analyses reveal interactions between the skin microbiota and skin metabolites in atopic dermatitis
topic atopic dermatitis
skin microbiome
skin metabolome
correlation analysis
purine metabolism
phenylalanine metabolism
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1349674/full
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