Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia

Abstract Background Preeclampsia is a pregnancy-specific disease leading to maternal and perinatal morbidity. Hypertension and inflammation are the main characteristics of preeclampsia. Many factors can lead to hypertension and inflammation, including gut microbiota which plays an important role in...

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Main Authors: Xianxian Liu, Xiaoming Zeng, Xing Li, Siming Xin, Feng Zhang, Faying Liu, Yang Zeng, Jilin Wu, Yang Zou, Xinwei Xiong
Format: Article
Language:English
Published: BMC 2024-04-01
Series:Journal of Translational Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12967-024-05143-5
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author Xianxian Liu
Xiaoming Zeng
Xing Li
Siming Xin
Feng Zhang
Faying Liu
Yang Zeng
Jilin Wu
Yang Zou
Xinwei Xiong
author_facet Xianxian Liu
Xiaoming Zeng
Xing Li
Siming Xin
Feng Zhang
Faying Liu
Yang Zeng
Jilin Wu
Yang Zou
Xinwei Xiong
author_sort Xianxian Liu
collection DOAJ
description Abstract Background Preeclampsia is a pregnancy-specific disease leading to maternal and perinatal morbidity. Hypertension and inflammation are the main characteristics of preeclampsia. Many factors can lead to hypertension and inflammation, including gut microbiota which plays an important role in hypertension and inflammation in humans. However, alterations to the gut microbiome and fecal metabolome, and their relationships in severe preeclampsia are not well known. This study aims to identify biomarkers significantly associated with severe preeclampsia and provide a knowledge base for treatments regulating the gut microbiome. Methods In this study, fecal samples were collected from individuals with severe preeclampsia and healthy controls for shotgun metagenomic sequencing to evaluate changes in gut microbiota composition. Quantitative polymerase chain reaction analysis was used to validate the reliability of our shotgun metagenomic sequencing results. Additionally, untargeted metabolomics analysis was performed to measure fecal metabolome concentrations. Results We identified several Lactobacillaceae that were significantly enriched in the gut of healthy controls, including Limosilactobacillus fermentum, the key biomarker distinguishing severe preeclampsia from healthy controls. Limosilactobacillus fermentum was significantly associated with shifts in KEGG Orthology (KO) genes and KEGG pathways of the gut microbiome in severe preeclampsia, such as flagellar assembly. Untargeted fecal metabolome analysis found that severe preeclampsia had higher concentrations of Phenylpropanoate and Agmatine. Increased concentrations of Phenylpropanoate and Agmatine were associated with the abundance of Limosilactobacillus fermentum. Furthermore, all metabolites with higher abundances in healthy controls were enriched in the arginine and proline metabolism pathway. Conclusion Our research indicates that changes in metabolites, possibly due to the gut microbe Limosilactobacillus fermentum, can contribute to the development of severe preeclampsia. This study provides insights into the interaction between gut microbiome and fecal metabolites and offers a basis for improving severe preeclampsia by modulating the gut microbiome.
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spelling doaj.art-792a4a6f451a4bd481ee44c94b2e6cd32024-04-21T11:28:39ZengBMCJournal of Translational Medicine1479-58762024-04-0122111210.1186/s12967-024-05143-5Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsiaXianxian Liu0Xiaoming Zeng1Xing Li2Siming Xin3Feng Zhang4Faying Liu5Yang Zeng6Jilin Wu7Yang Zou8Xinwei Xiong9Key Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalMedical Center of Burn Plastic and Wound Repair, The First Affiliated Hospital of Nanchang University, Jiangxi Medical College, Nanchang UniversityKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalKey Laboratory of Women’s Reproductive Health of Jiangxi Province, Jiangxi Maternal and Child Health HospitalInstitute of Biological Technology, Nanchang Normal UniversityAbstract Background Preeclampsia is a pregnancy-specific disease leading to maternal and perinatal morbidity. Hypertension and inflammation are the main characteristics of preeclampsia. Many factors can lead to hypertension and inflammation, including gut microbiota which plays an important role in hypertension and inflammation in humans. However, alterations to the gut microbiome and fecal metabolome, and their relationships in severe preeclampsia are not well known. This study aims to identify biomarkers significantly associated with severe preeclampsia and provide a knowledge base for treatments regulating the gut microbiome. Methods In this study, fecal samples were collected from individuals with severe preeclampsia and healthy controls for shotgun metagenomic sequencing to evaluate changes in gut microbiota composition. Quantitative polymerase chain reaction analysis was used to validate the reliability of our shotgun metagenomic sequencing results. Additionally, untargeted metabolomics analysis was performed to measure fecal metabolome concentrations. Results We identified several Lactobacillaceae that were significantly enriched in the gut of healthy controls, including Limosilactobacillus fermentum, the key biomarker distinguishing severe preeclampsia from healthy controls. Limosilactobacillus fermentum was significantly associated with shifts in KEGG Orthology (KO) genes and KEGG pathways of the gut microbiome in severe preeclampsia, such as flagellar assembly. Untargeted fecal metabolome analysis found that severe preeclampsia had higher concentrations of Phenylpropanoate and Agmatine. Increased concentrations of Phenylpropanoate and Agmatine were associated with the abundance of Limosilactobacillus fermentum. Furthermore, all metabolites with higher abundances in healthy controls were enriched in the arginine and proline metabolism pathway. Conclusion Our research indicates that changes in metabolites, possibly due to the gut microbe Limosilactobacillus fermentum, can contribute to the development of severe preeclampsia. This study provides insights into the interaction between gut microbiome and fecal metabolites and offers a basis for improving severe preeclampsia by modulating the gut microbiome.https://doi.org/10.1186/s12967-024-05143-5Severe preeclampsiaGut microbiomeMetagenomic sequencingFecal metabolomeBiomarkers
spellingShingle Xianxian Liu
Xiaoming Zeng
Xing Li
Siming Xin
Feng Zhang
Faying Liu
Yang Zeng
Jilin Wu
Yang Zou
Xinwei Xiong
Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
Journal of Translational Medicine
Severe preeclampsia
Gut microbiome
Metagenomic sequencing
Fecal metabolome
Biomarkers
title Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
title_full Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
title_fullStr Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
title_full_unstemmed Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
title_short Landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
title_sort landscapes of gut bacterial and fecal metabolic signatures and their relationship in severe preeclampsia
topic Severe preeclampsia
Gut microbiome
Metagenomic sequencing
Fecal metabolome
Biomarkers
url https://doi.org/10.1186/s12967-024-05143-5
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