Exploring the composition of placental microbiome and its potential origin in preterm birth.

IF 4.8 2区 医学 Q2 IMMUNOLOGY Frontiers in Cellular and Infection Microbiology Pub Date : 2025-01-16 eCollection Date: 2024-01-01 DOI:10.3389/fcimb.2024.1486409
Marwa Saadaoui, Mohamed Nadhir Djekidel, Selvasankar Murugesan, Manoj Kumar, Duaa Elhag, Parul Singh, Basirudeen Syed Ahamed Kabeer, Alexandra Katharina Marr, Tomoshige Kino, Tobias Brummaier, Rose McGready, François Nosten, Damien Chaussabel, Annalisa Terranegra, Souhaila Al Khodor
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Abstract

Introduction: For years, the placenta was believed to be sterile, but recent studies reveal it hosts a unique microbiome. Despite these findings, significant questions remain about the origins of the placental microbiome and its effects on pregnancy and fetal health. Some studies suggest it may originate from the vaginal tract, while others indicate that oral bacteria can enter the maternal bloodstream and seed the placenta. However, research analyzing the vaginal, oral, and placental microbiomes within the same cohort is lacking. Additionally, it's unclear whether the placental microbiome differs between healthy pregnancies and those with complications like preterm birth (PTB), which remains a leading cause of neonatal morbidity and mortality worldwide.

Methods: In this study, we performed 16S rRNA gene sequencing to investigate the composition of the oral and placental microbiome in samples collected from 18 women who experienced PTB and 36 matched controls who delivered at term (TB), all of whom were part of the Molecular Signature in Pregnancy (MSP) study. We leveraged on the multisite microbiome sampling from the MSP participants and on our previously published vaginal microbiome data to investigate the potential origins of the placental microbiome and assess whether its composition varies between healthy and complicated pregnancies.

Results and discussion: Our analysis revealed distinct profiles in the oral microbiome of PTB subjects compared to those who delivered at term. Specifically, we observed an increased abundance of Treponema maltophilum, Bacteroides sp, Mollicutes, Prevotella buccae, Leptotrichia, Prevotella_sp_Alloprevotella, in the PTB group. Importantly, Treponema maltophilum species showed higher abundance in the PTB group during the second trimester, suggesting its potential use as biomarkers. When we assessed the placenta microbiome composition, we found that Firmicutes, Bacteroidetes, Actinobacteria, and Proteobacteria were the most dominant phyla. Interestingly, microorganisms such as Ureaplasma urealyticum were more abundant in PTB placenta samples. Our findings suggest that the placenta microbiome could originate from the oral or vaginal cavities, with a notable increase in the crosstalk between the vaginal and placental sites in cases of PTB. Specifically, our data revealed that in PTB cases, the placental microbiome exhibited a closer resemblance to the vaginal microbiome, whereas in term pregnancies, the placental microbiome was similar to the oral microbiome.

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早产儿胎盘微生物群组成及其潜在来源的探讨。
多年来,人们一直认为胎盘是无菌的,但最近的研究表明,它拥有一种独特的微生物群。尽管有这些发现,胎盘微生物群的起源及其对妊娠和胎儿健康的影响仍然存在重大问题。一些研究表明,它可能起源于阴道,而另一些研究表明,口腔细菌可以进入母体的血液并播种胎盘。然而,在同一队列中分析阴道、口腔和胎盘微生物组的研究缺乏。此外,目前还不清楚健康妊娠和早产(PTB)等并发症之间的胎盘微生物群是否存在差异,早产仍是全球新生儿发病率和死亡率的主要原因。方法:在这项研究中,我们对18名患PTB的妇女和36名足月分娩的对照组的样本进行了16S rRNA基因测序,研究了口腔和胎盘微生物组的组成,这些样本都是妊娠分子特征(MSP)研究的一部分。我们利用来自MSP参与者的多点微生物组采样和我们之前发表的阴道微生物组数据来研究胎盘微生物组的潜在起源,并评估其组成是否在健康和复杂妊娠之间存在差异。结果和讨论:我们的分析显示,与足月分娩的患者相比,PTB患者的口腔微生物组具有明显的特征。具体来说,我们观察到在PTB组中,麦芽密螺旋体、拟杆菌、Mollicutes、buccae普雷沃氏菌、Leptotrichia、Prevotella_sp_Alloprevotella的丰度增加。重要的是,在妊娠中期,嗜麦芽密螺旋体在PTB组中显示出更高的丰度,这表明它可能用作生物标志物。当我们评估胎盘微生物组组成时,我们发现厚壁菌门、拟杆菌门、放线菌门和变形菌门是最占优势的门。有趣的是,在PTB胎盘样本中,解脲支原体等微生物更为丰富。我们的研究结果表明,胎盘微生物群可能起源于口腔或阴道腔,在PTB病例中,阴道和胎盘部位之间的串扰显著增加。具体来说,我们的数据显示,在PTB病例中,胎盘微生物组与阴道微生物组表现出更接近的相似性,而在足月妊娠中,胎盘微生物组与口腔微生物组相似。
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来源期刊
CiteScore
7.90
自引率
7.00%
发文量
1817
审稿时长
14 weeks
期刊介绍: Frontiers in Cellular and Infection Microbiology is a leading specialty journal, publishing rigorously peer-reviewed research across all pathogenic microorganisms and their interaction with their hosts. Chief Editor Yousef Abu Kwaik, University of Louisville is supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide. Frontiers in Cellular and Infection Microbiology includes research on bacteria, fungi, parasites, viruses, endosymbionts, prions and all microbial pathogens as well as the microbiota and its effect on health and disease in various hosts. The research approaches include molecular microbiology, cellular microbiology, gene regulation, proteomics, signal transduction, pathogenic evolution, genomics, structural biology, and virulence factors as well as model hosts. Areas of research to counteract infectious agents by the host include the host innate and adaptive immune responses as well as metabolic restrictions to various pathogenic microorganisms, vaccine design and development against various pathogenic microorganisms, and the mechanisms of antibiotic resistance and its countermeasures.
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