Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia

ABSTRACTPreeclampsia (PE), a pregnancy-specific syndrome, has been associated with the gut bacteriome. Here, to investigate the impact of the gut virome on the development of PE, we identified over 8,000 nonredundant viruses from the fecal metagenomes of 40 early-onset PE and 37 healthy pregnant wom...

Full description

Bibliographic Details
Main Authors: Li-Juan Lv, Ji-Ying Wen, Yue Zhang, Ruo-Chun Guo, Hui Li, Zhou-Ting Yi, Tian-Wen He, Min-Chai Chen, Yang Chen, Xiao-Yan Wu, Sheng-hui Li, Jian Kang, Ya-Ping Hou, Qiu-long Yan, Ai-Hua Yin
Format: Article
Language:English
Published: American Society for Microbiology 2024-04-01
Series:mSphere
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msphere.00676-23
_version_ 1797194052757618688
author Li-Juan Lv
Ji-Ying Wen
Yue Zhang
Ruo-Chun Guo
Hui Li
Zhou-Ting Yi
Tian-Wen He
Min-Chai Chen
Yang Chen
Xiao-Yan Wu
Sheng-hui Li
Jian Kang
Ya-Ping Hou
Qiu-long Yan
Ai-Hua Yin
author_facet Li-Juan Lv
Ji-Ying Wen
Yue Zhang
Ruo-Chun Guo
Hui Li
Zhou-Ting Yi
Tian-Wen He
Min-Chai Chen
Yang Chen
Xiao-Yan Wu
Sheng-hui Li
Jian Kang
Ya-Ping Hou
Qiu-long Yan
Ai-Hua Yin
author_sort Li-Juan Lv
collection DOAJ
description ABSTRACTPreeclampsia (PE), a pregnancy-specific syndrome, has been associated with the gut bacteriome. Here, to investigate the impact of the gut virome on the development of PE, we identified over 8,000 nonredundant viruses from the fecal metagenomes of 40 early-onset PE and 37 healthy pregnant women and profiled their abundances. Comparison and correlation analysis showed that PE-enriched viruses frequently connected to Blautia species enriched in PE. By contrast, bacteria linked to PE-depleted viruses were often the Bacteroidaceae members such as Bacteroides spp., Phocaeicola spp., Parabacteroides spp., and Alistipes shahii. In terms of viral function, PE-depleted viruses had auxiliary metabolic genes that participated in the metabolism of simple and complex polysaccharides, sulfur metabolism, lipopolysaccharide biosynthesis, and peptidoglycan biosynthesis, while PE-enriched viruses had a gene encoding cyclic pyranopterin monophosphate synthase, which seemed to be special, that participates in the biosynthesis of the molybdenum cofactor. Furthermore, the classification model based on gut viral signatures was developed to discriminate PE patients from healthy controls and showed an area under the receiver operating characteristic curve of 0.922 that was better than that of the bacterium-based model. This study opens up new avenues for further research, providing valuable insights into the PE gut virome and offering potential directions for future mechanistic and therapeutic investigations, with the ultimate goal of improving the diagnosis and management of PE.IMPORTANCEThe importance of this study lies in its exploration of the previously overlooked but potentially critical role of the gut virome in preeclampsia (PE). While the association between PE and the gut bacteriome has been recognized, this research takes a pioneering step into understanding how the gut virome, represented by over 8,000 nonredundant viruses, contributes to this condition. The findings reveal intriguing connections between PE-enriched viruses and specific gut bacteria, such as the prevalence of Blautia species in individuals with PE, contrasting with bacteria linked to PE-depleted viruses, including members of the Bacteroidaceae family. These viral interactions and associations provide a deeper understanding of the complex dynamics at play in PE.
first_indexed 2024-04-24T05:50:09Z
format Article
id doaj.art-74857f3b8e1248a789b32f345e503937
institution Directory Open Access Journal
issn 2379-5042
language English
last_indexed 2024-04-24T05:50:09Z
publishDate 2024-04-01
publisher American Society for Microbiology
record_format Article
series mSphere
spelling doaj.art-74857f3b8e1248a789b32f345e5039372024-04-23T13:00:39ZengAmerican Society for MicrobiologymSphere2379-50422024-04-019410.1128/msphere.00676-23Deep metagenomic characterization of the gut virome in pregnant women with preeclampsiaLi-Juan Lv0Ji-Ying Wen1Yue Zhang2Ruo-Chun Guo3Hui Li4Zhou-Ting Yi5Tian-Wen He6Min-Chai Chen7Yang Chen8Xiao-Yan Wu9Sheng-hui Li10Jian Kang11Ya-Ping Hou12Qiu-long Yan13Ai-Hua Yin14Medical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaDepartment of Obstetrics, Guangdong Women and Children Hospital, Guangzhou, ChinaPuensum Genetech Institute, Wuhan, ChinaPuensum Genetech Institute, Wuhan, ChinaDepartment of Obstetrics, Guangdong Women and Children Hospital, Guangzhou, ChinaDepartment of Obstetrics, Guangdong Women and Children Hospital, Guangzhou, ChinaMedical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaMedical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaMedical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaMedical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaPuensum Genetech Institute, Wuhan, ChinaDepartment of Microbiology, College of Basic Medical Science, Dalian Medical University, Dalian, ChinaMedical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaDepartment of Microbiology, College of Basic Medical Science, Dalian Medical University, Dalian, ChinaMedical Genetic Center, Guangdong Women and Children Hospital, Guangzhou, ChinaABSTRACTPreeclampsia (PE), a pregnancy-specific syndrome, has been associated with the gut bacteriome. Here, to investigate the impact of the gut virome on the development of PE, we identified over 8,000 nonredundant viruses from the fecal metagenomes of 40 early-onset PE and 37 healthy pregnant women and profiled their abundances. Comparison and correlation analysis showed that PE-enriched viruses frequently connected to Blautia species enriched in PE. By contrast, bacteria linked to PE-depleted viruses were often the Bacteroidaceae members such as Bacteroides spp., Phocaeicola spp., Parabacteroides spp., and Alistipes shahii. In terms of viral function, PE-depleted viruses had auxiliary metabolic genes that participated in the metabolism of simple and complex polysaccharides, sulfur metabolism, lipopolysaccharide biosynthesis, and peptidoglycan biosynthesis, while PE-enriched viruses had a gene encoding cyclic pyranopterin monophosphate synthase, which seemed to be special, that participates in the biosynthesis of the molybdenum cofactor. Furthermore, the classification model based on gut viral signatures was developed to discriminate PE patients from healthy controls and showed an area under the receiver operating characteristic curve of 0.922 that was better than that of the bacterium-based model. This study opens up new avenues for further research, providing valuable insights into the PE gut virome and offering potential directions for future mechanistic and therapeutic investigations, with the ultimate goal of improving the diagnosis and management of PE.IMPORTANCEThe importance of this study lies in its exploration of the previously overlooked but potentially critical role of the gut virome in preeclampsia (PE). While the association between PE and the gut bacteriome has been recognized, this research takes a pioneering step into understanding how the gut virome, represented by over 8,000 nonredundant viruses, contributes to this condition. The findings reveal intriguing connections between PE-enriched viruses and specific gut bacteria, such as the prevalence of Blautia species in individuals with PE, contrasting with bacteria linked to PE-depleted viruses, including members of the Bacteroidaceae family. These viral interactions and associations provide a deeper understanding of the complex dynamics at play in PE.https://journals.asm.org/doi/10.1128/msphere.00676-23preeclampsiagut viromegut microbiotaviral diversityviral functionpregnant women
spellingShingle Li-Juan Lv
Ji-Ying Wen
Yue Zhang
Ruo-Chun Guo
Hui Li
Zhou-Ting Yi
Tian-Wen He
Min-Chai Chen
Yang Chen
Xiao-Yan Wu
Sheng-hui Li
Jian Kang
Ya-Ping Hou
Qiu-long Yan
Ai-Hua Yin
Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
mSphere
preeclampsia
gut virome
gut microbiota
viral diversity
viral function
pregnant women
title Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
title_full Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
title_fullStr Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
title_full_unstemmed Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
title_short Deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
title_sort deep metagenomic characterization of the gut virome in pregnant women with preeclampsia
topic preeclampsia
gut virome
gut microbiota
viral diversity
viral function
pregnant women
url https://journals.asm.org/doi/10.1128/msphere.00676-23
work_keys_str_mv AT lijuanlv deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT jiyingwen deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT yuezhang deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT ruochunguo deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT huili deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT zhoutingyi deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT tianwenhe deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT minchaichen deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT yangchen deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT xiaoyanwu deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT shenghuili deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT jiankang deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT yapinghou deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT qiulongyan deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia
AT aihuayin deepmetagenomiccharacterizationofthegutviromeinpregnantwomenwithpreeclampsia