Landscapes of maternal and neonatal gut microbiome and plasma metabolome signatures and their interaction in gestational diabetes mellitus

IF 4.8 2区医学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY

Journal of Nutritional Biochemistry Pub Date : 2024-08-13 DOI:10.1016/j.jnutbio.2024.109716

Jieying Liu , Xiao Zhai , Lu Ding , Miao Yu , Qian Zhang , Juntao Liu , Yingna Song , Liangkun Ma , Xinhua Xiao

{"title":"Landscapes of maternal and neonatal gut microbiome and plasma metabolome signatures and their interaction in gestational diabetes mellitus","authors":"Jieying Liu , Xiao Zhai , Lu Ding , Miao Yu , Qian Zhang , Juntao Liu , Yingna Song , Liangkun Ma , Xinhua Xiao","doi":"10.1016/j.jnutbio.2024.109716","DOIUrl":null,"url":null,"abstract":"<div><p>Gestational diabetes mellitus (GDM) is prevalent among pregnant individuals and is linked to increased risks for both mothers and fetuses. Although GDM is known to cause disruptions in gut microbiota and metabolites, their potential transmission to the fetus has not been fully explored. This study aimed to characterize the similarities in microbial and metabolic signatures between mothers with GDM and their neonates as well as the interactions between these signatures. This study included 89 maternal-neonate pairs (44 in the GDM group and 45 in the normoglycemic group). We utilized 16S rRNA gene sequencing and untargeted metabolomics to analyze the gut microbiota and plasma metabolomics of mothers and neonates. Integrative analyses were performed to elucidate the interactions between these omics. Distinct microbial and metabolic signatures were observed in GDM mothers and their neonates compared to those in the normoglycemic group. Fourteen genera showed similar alterations across both groups. Metabolites linked to glucose, lipid, and energy metabolism were differentially influenced in GDM, with similar trends observed in both mothers and neonates in the GDM group. Network analysis indicated significant associations between <em>Qipengyuania</em> and metabolites related to bile acid metabolism in mothers and newborns. Furthermore, we observed a significant correlation between several genera and metabolites and clinical phenotypes in normoglycemic mothers and newborns, but these correlations were disrupted in the GDM group. Our findings suggest that GDM consistently affects both the microbiota and metabolome in mothers and neonates, thus elucidating the mechanism underlying metabolic transmission across generations. These insights contribute to knowledge regarding the multiomics interactions in GDM and underscore the need to further investigate the prenatal environmental impacts on offspring metabolism.</p></div>","PeriodicalId":16618,"journal":{"name":"Journal of Nutritional Biochemistry","volume":"134 ","pages":"Article 109716"},"PeriodicalIF":4.8000,"publicationDate":"2024-08-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Nutritional Biochemistry","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0955286324001487","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

Gestational diabetes mellitus (GDM) is prevalent among pregnant individuals and is linked to increased risks for both mothers and fetuses. Although GDM is known to cause disruptions in gut microbiota and metabolites, their potential transmission to the fetus has not been fully explored. This study aimed to characterize the similarities in microbial and metabolic signatures between mothers with GDM and their neonates as well as the interactions between these signatures. This study included 89 maternal-neonate pairs (44 in the GDM group and 45 in the normoglycemic group). We utilized 16S rRNA gene sequencing and untargeted metabolomics to analyze the gut microbiota and plasma metabolomics of mothers and neonates. Integrative analyses were performed to elucidate the interactions between these omics. Distinct microbial and metabolic signatures were observed in GDM mothers and their neonates compared to those in the normoglycemic group. Fourteen genera showed similar alterations across both groups. Metabolites linked to glucose, lipid, and energy metabolism were differentially influenced in GDM, with similar trends observed in both mothers and neonates in the GDM group. Network analysis indicated significant associations between Qipengyuania and metabolites related to bile acid metabolism in mothers and newborns. Furthermore, we observed a significant correlation between several genera and metabolites and clinical phenotypes in normoglycemic mothers and newborns, but these correlations were disrupted in the GDM group. Our findings suggest that GDM consistently affects both the microbiota and metabolome in mothers and neonates, thus elucidating the mechanism underlying metabolic transmission across generations. These insights contribute to knowledge regarding the multiomics interactions in GDM and underscore the need to further investigate the prenatal environmental impacts on offspring metabolism.

查看原文本刊更多论文

妊娠期糖尿病患者的母体和新生儿肠道微生物组和血浆代谢组特征及其相互作用。

背景：妊娠期糖尿病（GDM）在孕妇中很普遍，它与母亲和胎儿的风险增加有关。虽然已知 GDM 会导致肠道微生物群和代谢物的紊乱，但尚未充分探讨它们对胎儿的潜在影响。本研究旨在描述 GDM 母亲和新生儿之间微生物和代谢特征的相似性，以及这些特征之间的相互作用：这项研究包括 89 对母婴（GDM 组 44 对，正常血糖组 45 对）。我们利用 16S rRNA 基因测序和非靶向代谢组学分析了母亲和新生儿的肠道微生物群和血浆代谢组学。研究人员进行了整合分析，以阐明这些组学之间的相互作用：结果：与正常血糖组相比，在 GDM 母亲及其新生儿中观察到了不同的微生物和代谢特征。两组中有 14 个菌属发生了类似的变化。与葡萄糖、脂质和能量代谢有关的代谢物在 GDM 中受到不同程度的影响，在 GDM 组的母亲和新生儿中观察到类似的趋势。网络分析显示，芪苈强心丸与母亲和新生儿体内胆汁酸代谢相关代谢物之间存在明显关联。此外，我们还观察到，在血糖正常的母亲和新生儿中，一些属和代谢物与临床表型之间存在明显的相关性，但在 GDM 组中，这些相关性被打破：我们的研究结果表明，GDM 会持续影响母亲和新生儿的微生物群和代谢组，从而阐明了跨代代谢传递的机制。这些见解有助于了解 GDM 的多组学相互作用，并强调有必要进一步研究产前环境对后代代谢的影响。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Journal of Nutritional Biochemistry 医学-生化与分子生物学

CiteScore

9.50

自引率

3.60%

发文量

237

审稿时长

68 days

期刊介绍： Devoted to advancements in nutritional sciences, The Journal of Nutritional Biochemistry presents experimental nutrition research as it relates to: biochemistry, molecular biology, toxicology, or physiology. Rigorous reviews by an international editorial board of distinguished scientists ensure publication of the most current and key research being conducted in nutrition at the cellular, animal and human level. In addition to its monthly features of critical reviews and research articles, The Journal of Nutritional Biochemistry also periodically publishes emerging issues, experimental methods, and other types of articles.