Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes

Abstract Background Microgenderome or arguably more accurately microsexome refers to studies on sexual dimorphism of human microbiomes aimed at investigating bidirectional interactions between human microbiomes, sex hormones, and immune systems. It is important because of its implications to disease...

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Main Author: Zhanshan Sam Ma
Format: Article
Language:English
Published: BMC 2024-12-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-024-02025-6
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author Zhanshan Sam Ma
author_facet Zhanshan Sam Ma
author_sort Zhanshan Sam Ma
collection DOAJ
description Abstract Background Microgenderome or arguably more accurately microsexome refers to studies on sexual dimorphism of human microbiomes aimed at investigating bidirectional interactions between human microbiomes, sex hormones, and immune systems. It is important because of its implications to disease susceptibility and therapy, in which men and women demonstrate divergence in many diseases especially autoimmune diseases. In a previous report [1], we presented analyses of several key ecological aspects of microgenderome by leveraging the large datasets of the HMP (human microbiome project) but failed to offer species-level composition differences such as sexually unique species (US) and enriched species (ES). Existing approaches, for such tasks, including differential species relative abundance analysis and differential network analysis, possess certain limitations given that virtually all rely on species abundance alone or are univariate, while ignoring species distribution information across samples. Obviously, it is both species abundance and distribution that shape/drive the structure and dynamics of human microbiomes, and both should be equally responsible for the universal heterogeneity of microbiomes including the sexual dimorphism. Results Here, we fill the gap by taking advantages of a recently developed computational algorithm, species specificity, and specificity diversity (SSD) framework (refer to the companion article) to reanalyze the HMP and complementary seminovaginal microbiome datasets. The SSD framework can randomly search and catalogue the sexually specific unique/enriched species with statistical rigor, guided by species specificity (a synthetic metric of abundance and distribution) and specificity diversity (SD). The SSD framework reveals that men seem to have more unique species than women in their gut and reproductive system microbiomes, but women seem to have more unique species than men in the airway, oral, and skin microbiomes, which is likely due to sexual dimorphism in the hormone and immune systems. We further investigate co-dependency and heterogeneity of those sexually unique/enriched species across 15 body sites, with core/periphery network analyses. Conclusions This study not only produced sexually unique/enriched species in the human microbiomes and analyzed their codependency and heterogeneity but also further validated the robustness of the SSD framework presented in the companion article, by performing all negative control tests based on the HMP gut microbiome samples.
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spelling doaj-art-b66dbac713214352a6a87d061bf578192025-01-26T12:52:34ZengBMCBMC Biology1741-70072024-12-0122111710.1186/s12915-024-02025-6Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomesZhanshan Sam Ma0Computational Biology and Medical Ecology Lab, Kunming Institute of Zoology, Chinese Academy of SciencesAbstract Background Microgenderome or arguably more accurately microsexome refers to studies on sexual dimorphism of human microbiomes aimed at investigating bidirectional interactions between human microbiomes, sex hormones, and immune systems. It is important because of its implications to disease susceptibility and therapy, in which men and women demonstrate divergence in many diseases especially autoimmune diseases. In a previous report [1], we presented analyses of several key ecological aspects of microgenderome by leveraging the large datasets of the HMP (human microbiome project) but failed to offer species-level composition differences such as sexually unique species (US) and enriched species (ES). Existing approaches, for such tasks, including differential species relative abundance analysis and differential network analysis, possess certain limitations given that virtually all rely on species abundance alone or are univariate, while ignoring species distribution information across samples. Obviously, it is both species abundance and distribution that shape/drive the structure and dynamics of human microbiomes, and both should be equally responsible for the universal heterogeneity of microbiomes including the sexual dimorphism. Results Here, we fill the gap by taking advantages of a recently developed computational algorithm, species specificity, and specificity diversity (SSD) framework (refer to the companion article) to reanalyze the HMP and complementary seminovaginal microbiome datasets. The SSD framework can randomly search and catalogue the sexually specific unique/enriched species with statistical rigor, guided by species specificity (a synthetic metric of abundance and distribution) and specificity diversity (SD). The SSD framework reveals that men seem to have more unique species than women in their gut and reproductive system microbiomes, but women seem to have more unique species than men in the airway, oral, and skin microbiomes, which is likely due to sexual dimorphism in the hormone and immune systems. We further investigate co-dependency and heterogeneity of those sexually unique/enriched species across 15 body sites, with core/periphery network analyses. Conclusions This study not only produced sexually unique/enriched species in the human microbiomes and analyzed their codependency and heterogeneity but also further validated the robustness of the SSD framework presented in the companion article, by performing all negative control tests based on the HMP gut microbiome samples.https://doi.org/10.1186/s12915-024-02025-6MicrogenderomeSpecies specificity and specificity diversity (SSD) frameworkSexually unique species (US)Sexually enriched species (ES)Species specificity (SS)Specificity diversity (SD)
spellingShingle Zhanshan Sam Ma
Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes
BMC Biology
Microgenderome
Species specificity and specificity diversity (SSD) framework
Sexually unique species (US)
Sexually enriched species (ES)
Species specificity (SS)
Specificity diversity (SD)
title Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes
title_full Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes
title_fullStr Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes
title_full_unstemmed Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes
title_short Revisiting microgenderome: detecting and cataloguing sexually unique and enriched species in human microbiomes
title_sort revisiting microgenderome detecting and cataloguing sexually unique and enriched species in human microbiomes
topic Microgenderome
Species specificity and specificity diversity (SSD) framework
Sexually unique species (US)
Sexually enriched species (ES)
Species specificity (SS)
Specificity diversity (SD)
url https://doi.org/10.1186/s12915-024-02025-6
work_keys_str_mv AT zhanshansamma revisitingmicrogenderomedetectingandcataloguingsexuallyuniqueandenrichedspeciesinhumanmicrobiomes