Remodeling of the maternal gut microbiome during pregnancy is shaped by parity.

Remodeling of the maternal gut microbiome during pregnancy is shaped by parity.
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DOI:
10.1186/s40168-021-01089-8
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发表时间:
2021-06-27
期刊:
影响因子:
15.5
通讯作者:
Beiting DP
Beiting DP
中科院分区:
生物学1区
文献类型:
--
作者:
Berry ASF;Pierdon MK;Misic AM;Sullivan MC;O'Brien K;Chen Y;Murray SJ;Ramharack LA;Baldassano RN;Parsons TD;Beiting DP

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母体微生物组已成为妊娠健康和结局的重要因素,并与早产和后代发病风险相关。流行病学证据还指出,连续妊娠(称为母产)是早产、婴儿死亡率和新生儿生长受损的危险因素。尽管母体微生物组和胎次都与母婴健康相关,但胎次对微生物组的影响在很大程度上仍未被探索,部分原因是研究人类胎次的挑战。通过同步妊娠和对猪微生物组的密集纵向监测,我们描述了妊娠期间的微生物组轨迹,并确定胎次调节该轨迹的程度。我们发现,微生物组在妊娠期间会发生可重复的变化,并且随着胎次的增加,这种重塑发生得更快。分娩时,胎次与多种细菌的相对丰度有关,包括布氏密螺旋体、解淀粉乳杆菌和罗伊氏乳杆菌。在 18 个母子“四方体”(每个方体由一头母猪和三头仔猪组成)中进行的菌株追踪发现,母猪产次与婴儿出生 10 天后肠道中阿克曼氏菌、粪普氏菌和弯曲杆菌水平的变化有关。总的来说,这些结果表明胎次是调节妊娠期间肠道微生物组的重要环境因素,并强调了猪模型在研究母婴健康微生物组方面的实用性。此外,我们的数据表明,胎次的影响超出了母亲的范围,并且与生命早期定植于后代肠道的细菌群落的变化有关。我们在母亲和后代中鉴定为与胎次相关的细菌种类已被证明会影响其他系统中的宿主代谢,这增加了这种变化可能影响宿主营养物质获取或利用的可能性。这些发现与我们观察到的即使是细微的胎次差异也与微生物组变化相关的观察结果相结合,强调了在妊娠期和婴儿期人类微生物组研究的设计和分析中考虑胎次的重要性。视频摘要 在线版本包含可在 10.1186/s40168-021-01089-8 获取的补充材料。
The maternal microbiome has emerged as an important factor in gestational health and outcome and is associated with risk of preterm birth and offspring morbidity. Epidemiological evidence also points to successive pregnancies—referred to as maternal parity—as a risk factor for preterm birth, infant mortality, and impaired neonatal growth. Despite the fact that both the maternal microbiome and parity are linked to maternal-infant health, the impact of parity on the microbiome remains largely unexplored, in part due to the challenges of studying parity in humans. Using synchronized pregnancies and dense longitudinal monitoring of the microbiome in pigs, we describe a microbiome trajectory during pregnancy and determine the extent to which parity modulates this trajectory. We show that the microbiome changes reproducibly during gestation and that this remodeling occurs more rapidly as parity increases. At the time of parturition, parity was linked to the relative abundance of several bacterial species, including Treponema bryantii, Lactobacillus amylovorus, and Lactobacillus reuteri. Strain tracking carried out in 18 maternal-offspring “quadrads”—each consisting of one mother sow and three piglets—linked maternal parity to altered levels of Akkermansia muciniphila, Prevotella stercorea, and Campylobacter coli in the infant gut 10 days after birth. Collectively, these results identify parity as an important environmental factor that modulates the gut microbiome during pregnancy and highlight the utility of a swine model for investigating the microbiome in maternal-infant health. In addition, our data show that the impact of parity extends beyond the mother and is associated with alterations in the community of bacteria that colonize the offspring gut early in life. The bacterial species we identified as parity-associated in the mother and offspring have been shown to influence host metabolism in other systems, raising the possibility that such changes may influence host nutrient acquisition or utilization. These findings, taken together with our observation that even subtle differences in parity are associated with microbiome changes, underscore the importance of considering parity in the design and analysis of human microbiome studies during pregnancy and in infants. Video abstract The online version contains supplementary material available at 10.1186/s40168-021-01089-8.
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