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Gut microbiota
Original research
Landscape of the gut mycobiome dynamics during pregnancy and its relationship with host metabolism and pregnancy health
  1. Yuanqing Fu1,2,3,
  2. Wanglong Gou1,2,3,
  3. Ping Wu4,
  4. Yuwei Lai4,
  5. Xinxiu Liang2,3,
  6. Ke Zhang2,3,
  7. Menglei Shuai2,3,
  8. Jun Tang2,3,
  9. Zelei Miao2,3,
  10. Jieteng Chen2,3,
  11. Jiaying Yuan5,
  12. Bin Zhao6,
  13. Yunhaonan Yang7,
  14. Xiaojuan Liu8,
  15. Yayi Hu9,
  16. An Pan4,
  17. Xiong-Fei Pan7,10,11,
  18. Ju-Sheng Zheng1,2,3,12,13
  1. 1 Affiliated Hangzhou First People’s Hospital, School of Medicine, Westlake University, Hangzhou, China
  2. 2 Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, China
  3. 3 Research Center for Industries of the Future, School of Life Sciences, Westlake University, Hangzhou, China
  4. 4 Department of Epidemiology and Biostatistics, Ministry of Education Key Laboratory of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
  5. 5 Department of Science and Education, Shuangliu Maternal and Child Health Hospital, Chengdu, China
  6. 6 Antenatal Care Clinics, Shuangliu Maternal and Child Health Hospital, Chengdu, China
  7. 7 Section of Epidemiology and Population Health & Department of Obstetrics and Gynecology, Ministry of Education Key Laboratory of Birth Defects and Related Diseases of Women and Children & National Medical Products Administration Key Laboratory for Technical Research on Drug Products In Vitro and In Vivo Correlation, West China Second University Hospital, Sichuan University, Chengdu, China
  8. 8 Department of Laboratory Medicine, Ministry of Education Key Laboratory of Birth Defects and Related Diseases of Women and Children, West China Second University Hospital, Sichuan University, Chengdu, China
  9. 9 Department of Obstetrics and Gynecology, Ministry of Education Key Laboratory of Birth Defects and Related Diseases of Women and Children, West China Second University Hospital, Sichuan University, Chengdu, China
  10. 10 Shuangliu Institute of Women's and Children's Health, Shuangliu Maternal and Child Health Hospital, Chengdu, China
  11. 11 West China Biomedical Big Data Center, West China Hospital, Sichuan University, Chengdu, China
  12. 12 Institute of Basic Medical Sciences, Westlake Institute for Advanced Study, Hangzhou, China
  13. 13 Zhejiang Key Laboratory of Multi-Omics in Infection and Immunity, Center for Infectious Disease Research, School of Medicine, Westlake University, Hangzhou, China
  1. Correspondence to Professor Ju-Sheng Zheng, School of Medicine, Westlake University, Hangzhou 310030, Zhejiang, China; zhengjusheng{at}westlake.edu.cn; Professor Xiong-Fei Pan, West China Second University Hospital, Sichuan University, Chengdu 610041, China; pxiongfei{at}scu.edu.cn; Professor An Pan, Huazhong University of Science and Technology, Wuhan 430030, China; panan{at}hust.edu.cn

Abstract

Objective The remodelling of gut mycobiome (ie, fungi) during pregnancy and its potential influence on host metabolism and pregnancy health remains largely unexplored. Here, we aim to examine the characteristics of gut fungi in pregnant women, and reveal the associations between gut mycobiome, host metabolome and pregnancy health.

Design Based on a prospective birth cohort in central China (2017 to 2020): Tongji-Huaxi-Shuangliu Birth Cohort, we included 4800 participants who had available ITS2 sequencing data, dietary information and clinical records during their pregnancy. Additionally, we established a subcohort of 1059 participants, which included 514 women who gave birth to preterm, low birthweight or macrosomia infants, as well as 545 randomly selected controls. In this subcohort, a total of 750, 748 and 709 participants had ITS2 sequencing data, 16S sequencing data and serum metabolome data available, respectively, across all trimesters.

Results The composition of gut fungi changes dramatically from early to late pregnancy, exhibiting a greater degree of variability and individuality compared with changes observed in gut bacteria. The multiomics data provide a landscape of the networks among gut mycobiome, biological functionality, serum metabolites and pregnancy health, pinpointing the link between Mucor and adverse pregnancy outcomes. The prepregnancy overweight status is a key factor influencing both gut mycobiome compositional alteration and the pattern of metabolic remodelling during pregnancy.

Conclusion This study provides a landscape of gut mycobiome dynamics during pregnancy and its relationship with host metabolism and pregnancy health, which lays the foundation of the future gut mycobiome investigation for healthy pregnancy.

  • INTESTINAL MICROBIOLOGY

Data availability statement

Data are available in a public, open access repository. The raw data of ITS2, 16S and metagenomic sequencing in this study have been deposited in the Genome Sequence Archive (GSA) (https://ngdc.cncb.ac.cn/gsa/) at accession number CRA014764; CRA014766; CRA014529. Analysis R codes, Stata codes as well as the annotation pipelines for gut fungi, gut bacteria and gut microbial function are available via https://github.com/nutrition-westlake/THSBC-gut_fungi.Other data sets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/gutjnl-2024-332260

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    Data availability statement

    Data are available in a public, open access repository. The raw data of ITS2, 16S and metagenomic sequencing in this study have been deposited in the Genome Sequence Archive (GSA) (https://ngdc.cncb.ac.cn/gsa/) at accession number CRA014764; CRA014766; CRA014529. Analysis R codes, Stata codes as well as the annotation pipelines for gut fungi, gut bacteria and gut microbial function are available via https://github.com/nutrition-westlake/THSBC-gut_fungi.Other data sets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.

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    Footnotes

    • YF, WG, PW and YL are joint first authors.

    • X @zheng_jusheng

    • YF, WG, PW and YL contributed equally.

    • Contributors J-SZ, AP, X-FP and YF conceived the study concept and design. YF, WG, PW and YL analysed the data. PW, YL, JY, BZ, YY, XL, YH contributed to the field work, data collection and data curation. YF, KZ, XL, MS, JT, ZM and JC contributed to visualisation of the data. YF and J-SZ wrote the first draft of the manuscript. AP and X-FP contributed to the critical revision of the manuscript. YF, WG, PW and YL contributed equally to the work. All authors approved the final version of the manuscript for publication. J-SZ, AP and X-FP are the guarantors of this work and, as such, had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

    • Funding This study was funded by the National Key R&D Program of China (2022YFA1303900, 2023YFC3606300 and 2022YFC3600600), the National Natural Science Foundation of China (82103826,82073529, U21A20427, 82325043, 81930124, 82192902, 82021005 and 92374112), 'Pioneer' and 'Leading goose' R&D Program of Zhejiang (2022C03102), Zhejiang Provincial Natural Science Foundation of China (LQ21H260002), the Research Program of Westlake Laboratory of Life Sciences and Biomedicine (202208012), the Fundamental Research Funds for the Central Universities (YJ202346), China Postdoctoral Science Foundation (2023M733177, 2022M722833). The funders had no role in collecting data, study design, interpretation of data or the decision to submit the manuscript for publication.

    • Competing interests None declared.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.