Sex differences in the oral microbiome, host traits, and their causal relationships

Xiaomin Liu; Xin Tong; Zhuye Jie; Jie Zhu; Liu Tian; Qiang Sun; Yanmei Ju; Leying Zou; Haorong Lu; Xuemei Qiu; Qiang Li; Yunli Liao; Heng Lian; Yong Zuo; Xiaomin Chen; Weiqiao Rao; Yan Ren; Yuan Wang; Jin Zi; Rong Wang; Xun Xu; Huanming Yang; Jian Wang; Yang Zong; Weibin Liu; Yong Hou; Xin Jin; Liang Xiao; Karsten Kristiansen; Huijue Jia; Tao Zhang

doi:10.1016/j.isci.2022.105839

Sex differences in the oral microbiome, host traits, and their causal relationships

Xiaomin Liu, Xin Tong, Zhuye Jie, Jie Zhu, Liu Tian, Qiang Sun, Yanmei Ju, Leying Zou, Haorong Lu, Xuemei Qiu, Qiang Li, Yunli Liao, Heng Lian, Yong Zuo, Xiaomin Chen, Weiqiao Rao, Yan Ren, Yuan Wang, Jin Zi, Rong WangXun Xu, Huanming Yang, Jian Wang, Yang Zong, Weibin Liu, Yong Hou, Xin Jin, Liang Xiao, Karsten Kristiansen^*, Huijue Jia, Tao Zhang

^*Corresponding author for this work

Genome Research and Molecular Bio Medicine

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

The oral microbiome has been implicated in a growing number of diseases; however, determinants of the oral microbiome and their roles remain elusive. Here, we investigated the oral (saliva and tongue dorsum) metagenome, the whole genome, and other omics data in a total of 4,478 individuals and demonstrated that the oral microbiome composition and its major contributing host factors significantly differed between sexes. We thus conducted a sex-stratified metagenome-genome-wide-association study (M-GWAS) and identified 11 differential genetic associations with the oral microbiome (p_{sex-difference} < 5 × 10⁻⁸). Furthermore, we performed sex-stratified Mendelian randomization (MR) analyses and identified abundant causalities between the oral microbiome and serum metabolites. Notably, sex-specific microbes-hormonal interactions explained the mostly observed sex hormones differences such as the significant causalities enrichments for aldosterone in females and androstenedione in males. These findings illustrate the necessity of sex stratification and deepen our understanding of the interplay between the oral microbiome and serum metabolites.

Original language	English
Article number	105839
Journal	iScience
Volume	26
Issue number	1
Number of pages	23
ISSN	2589-0042
DOIs	https://doi.org/10.1016/j.isci.2022.105839
Publication status	Published - 2023

Bibliographical note

Publisher Copyright:
© 2022 The Author(s)

Keywords

Microbial metabolism
Microbiome
Oral microbiology

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10.1016/j.isci.2022.105839Licence: CC BY-NC-ND

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Cite this

Liu, X, Tong, X, Jie, Z, Zhu, J, Tian, L, Sun, Q, Ju, Y, Zou, L, Lu, H, Qiu, X, Li, Q, Liao, Y, Lian, H, Zuo, Y, Chen, X, Rao, W, Ren, Y, Wang, Y, Zi, J, Wang, R, Xu, X, Yang, H, Wang, J, Zong, Y, Liu, W, Hou, Y, Jin, X, Xiao, L, Kristiansen, K, Jia, H & Zhang, T 2023, 'Sex differences in the oral microbiome, host traits, and their causal relationships', iScience, vol. 26, no. 1, 105839. https://doi.org/10.1016/j.isci.2022.105839

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abstract = "The oral microbiome has been implicated in a growing number of diseases; however, determinants of the oral microbiome and their roles remain elusive. Here, we investigated the oral (saliva and tongue dorsum) metagenome, the whole genome, and other omics data in a total of 4,478 individuals and demonstrated that the oral microbiome composition and its major contributing host factors significantly differed between sexes. We thus conducted a sex-stratified metagenome-genome-wide-association study (M-GWAS) and identified 11 differential genetic associations with the oral microbiome (psex-difference < 5 × 10−8). Furthermore, we performed sex-stratified Mendelian randomization (MR) analyses and identified abundant causalities between the oral microbiome and serum metabolites. Notably, sex-specific microbes-hormonal interactions explained the mostly observed sex hormones differences such as the significant causalities enrichments for aldosterone in females and androstenedione in males. These findings illustrate the necessity of sex stratification and deepen our understanding of the interplay between the oral microbiome and serum metabolites.",

keywords = "Microbial metabolism, Microbiome, Oral microbiology",

author = "Xiaomin Liu and Xin Tong and Zhuye Jie and Jie Zhu and Liu Tian and Qiang Sun and Yanmei Ju and Leying Zou and Haorong Lu and Xuemei Qiu and Qiang Li and Yunli Liao and Heng Lian and Yong Zuo and Xiaomin Chen and Weiqiao Rao and Yan Ren and Yuan Wang and Jin Zi and Rong Wang and Xun Xu and Huanming Yang and Jian Wang and Yang Zong and Weibin Liu and Yong Hou and Xin Jin and Liang Xiao and Karsten Kristiansen and Huijue Jia and Tao Zhang",

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AU - Liu, Xiaomin

AU - Tong, Xin

AU - Jie, Zhuye

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AU - Tian, Liu

AU - Sun, Qiang

AU - Ju, Yanmei

AU - Zou, Leying

AU - Lu, Haorong

AU - Qiu, Xuemei

AU - Li, Qiang

AU - Liao, Yunli

AU - Lian, Heng

AU - Zuo, Yong

AU - Chen, Xiaomin

AU - Rao, Weiqiao

AU - Ren, Yan

AU - Wang, Yuan

AU - Zi, Jin

AU - Wang, Rong

AU - Xu, Xun

AU - Yang, Huanming

AU - Wang, Jian

AU - Zong, Yang

AU - Liu, Weibin

AU - Hou, Yong

AU - Jin, Xin

AU - Xiao, Liang

AU - Kristiansen, Karsten

AU - Jia, Huijue

AU - Zhang, Tao

PY - 2023

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N2 - The oral microbiome has been implicated in a growing number of diseases; however, determinants of the oral microbiome and their roles remain elusive. Here, we investigated the oral (saliva and tongue dorsum) metagenome, the whole genome, and other omics data in a total of 4,478 individuals and demonstrated that the oral microbiome composition and its major contributing host factors significantly differed between sexes. We thus conducted a sex-stratified metagenome-genome-wide-association study (M-GWAS) and identified 11 differential genetic associations with the oral microbiome (psex-difference < 5 × 10−8). Furthermore, we performed sex-stratified Mendelian randomization (MR) analyses and identified abundant causalities between the oral microbiome and serum metabolites. Notably, sex-specific microbes-hormonal interactions explained the mostly observed sex hormones differences such as the significant causalities enrichments for aldosterone in females and androstenedione in males. These findings illustrate the necessity of sex stratification and deepen our understanding of the interplay between the oral microbiome and serum metabolites.

AB - The oral microbiome has been implicated in a growing number of diseases; however, determinants of the oral microbiome and their roles remain elusive. Here, we investigated the oral (saliva and tongue dorsum) metagenome, the whole genome, and other omics data in a total of 4,478 individuals and demonstrated that the oral microbiome composition and its major contributing host factors significantly differed between sexes. We thus conducted a sex-stratified metagenome-genome-wide-association study (M-GWAS) and identified 11 differential genetic associations with the oral microbiome (psex-difference < 5 × 10−8). Furthermore, we performed sex-stratified Mendelian randomization (MR) analyses and identified abundant causalities between the oral microbiome and serum metabolites. Notably, sex-specific microbes-hormonal interactions explained the mostly observed sex hormones differences such as the significant causalities enrichments for aldosterone in females and androstenedione in males. These findings illustrate the necessity of sex stratification and deepen our understanding of the interplay between the oral microbiome and serum metabolites.

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