Visualization of microbes by 16S in situ hybridization in term and preterm placentas without intraamniotic infection

Seferovic, Maxim D.; Pace, Ryan M.; Carroll, Matthew; Belfort, Benjamin D.; Major, Angela; Chu, Derrick M.; Racusin, Diana A.; Castro, Eumenia; Muldrew, Kenneth L.; Versalovic, James; Aagaard, Kjersti M.

doi:10.1016/j.ajog.2019.04.036

Cited by 100 publications

(106 citation statements)

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“…Staphylococcus is a genus of bacteria commonly associated with mammalian skin and mucosal surfaces (91). It was detected in a preliminary molecular survey of the fetus and placenta of the Japanese macaque (85) and it has also been reported in numerous DNA sequence-based investigations of the human placenta (31–38, 41–43). However, Staphylococcus has also been identified as a background DNA contaminant in sequence-based studies (48), including in several prior studies of the human placenta (39, 57, 62).…”

Section: Discussioncontrasting

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Lack of evidence for microbiota in the placental and fetal tissues of rhesus macaques

Theis

Romero

Winters

et al. 2020

Preprint

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ABSTRACTThe prevailing paradigm in obstetrics has been the sterile womb hypothesis. However, some are asserting that the placenta, intra-amniotic environment, and fetus harbor microbial communities. The objective of this study was to determine if the fetal and placental tissues of rhesus macaques harbor viable bacterial communities. Fetal, placental, and uterine wall samples were obtained from cesarean deliveries without labor (∼130/166 days gestation). The presence of viable bacteria in the fetal intestine and placenta was investigated through culture. The bacterial burden and profile of the placenta, umbilical cord, and fetal brain, heart, liver, and colon were determined through quantitative real-time PCR and DNA sequencing. These data were compared with those of the uterine wall, as well as to negative and positive technical controls. Bacterial cultures of fetal and placental tissues yielded only a single colony of Cutibacterium acnes. This bacterium was detected at a low relative abundance (0.02%) in the 16S rRNA gene profile of the villous tree sample from which it was cultured, yet it was also identified in 12/29 background technical controls. The bacterial burden and profile of fetal and placental tissues did not exceed or differ from those of background technical controls. In contrast, the bacterial burden and profiles of positive controls exceeded and differed from those of background controls. Among the macaque samples, distinct microbial signals were limited to the uterine wall. Therefore, using multiple modes of microbiologic inquiry, there was not consistent evidence of viable bacterial communities in the fetal and placental tissues of rhesus macaques.IMPORTANCEMicrobial invasion of the amniotic cavity (i.e. intra-amniotic infection) has been causally linked to pregnancy complications, especially preterm birth. Therefore, if the placenta and the fetus are typically populated by low biomass yet viable microbial communities, current understanding of the role of microbes in reproduction and pregnancy outcomes will need to be fundamentally reconsidered. Could these communities be of benefit by competitively excluding potential pathogens or priming the fetal immune system for the microbial bombardment it will experience upon delivery? If so, what properties (e.g. microbial load, community membership) of these microbial communities preclude versus promote intra-amniotic infection? Given the ramifications of the in utero colonization hypothesis, critical evaluation is required. In this study, using multiple modes of microbiologic inquiry (i.e. culture, qPCR, DNA sequencing) and controlling for potential background DNA contamination, we did not find consistent evidence for microbial communities in the placenta and fetal tissues of rhesus macaques.

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Section: Discussioncontrasting

(Expert classified)

Lack of evidence for microbiota in the placental and fetal tissues of rhesus macaques

Theis

Romero

Winters

et al. 2020

Preprint

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“…The maternal microbiota affects the development of the intestinal immune system already in the fetal period 4 . This is mediated by circulating microbial metabolites 4 and possibly also by small numbers of microbial cells translocating to the fetus via placenta [5][6][7] . The major microbial colonization occurs at birth.…”

Section: Introductionmentioning

confidence: 99%

The composition of the perinatal intestinal microbiota in horse

Husso

Jalanka

Alipour

et al. 2019

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The establishment of the intestinal microbiota is critical for the digestive and immune systems. We studied the early development of the microbiota in horse, a hindgut fermenter, from birth until 7 days of age, by qPCR and 16S rRNA gene amplicon sequencing. To evaluate initial sources of foal microbiota, we characterized dam fecal, vaginal and oral microbiotas. We utilised an amplicon sequence variant (ASV) based pipeline to maximize resolution and reproducibility. Stringent ASV filtering based on prevalence and abundance in samples and controls purged reagent contaminants while preserving intestinal taxa. The newborn rectum contained small amounts of diverse bacterial DNA, with a profile closer to mare feces and vagina than mouth. 24 hours after birth, the intestine was colonized by Firmicutes and Proteobacteria, some foals dominated by a single genus. At day 7, the phylum-level composition resembled adult feces but genera were different. The mare vaginal microbiota contributed to 24 h and 7 day microbiotas. It contained few lactobacilli, with Corynebacterium, Porphyromonas, Campylobacter and Helcococcus as the most abundant genera. In the oral mucosa, Gemella was extremely abundant. Our observations suggest that bacteria or bacterial components translocate to the equine fetus, but the intestinal microbiota changes rapidly after birth.

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“…In our data, the L. iners versus L. crispatus shift was apparent in women with past pregnancy, and L. iners interestingly showed a negative association with number of spontaneous abortions (Figure 7). L. iners and other Lactobacilli have been detected in the placenta (Aagaard et al, 2014; de Goffau et al, 2019; Lannon et al, 2019; Macklaim et al, 2011; Seferovic et al, 2019), amniotic fluid, nasal and pharyngeal sites (Boeck et al; Wang et al, 2018a). Aldosterone, a major mineralocorticoid for which we observe association with potentially beneficial bacteria in the gut microbiome in an accompanying study (Jie et al, 2019), positively associated with L. crispatus in the vagino-cervical microbiome, while a precursor for aldosterone, corticosterone, positively associated with L. iners (Figure 7).…”

Section: Discussionmentioning

confidence: 99%

The vagino-cervical microbiome as a woman’s life history

Jie

Liang

et al. 2019

Preprint

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The vagina contains at least a billion microbial cells, which are dominated byLactobacilli. Here we perform metagenomic shotgun sequencing on cervical samples from 1148 women. Factors such as pregnancy, delivery histories and breast-feeding were all more important than menstrual cycle in shaping the microbiome. Bifidobacterium breve was seen with older age at sexual debut;Lactobacillus crispatus negatively correlated with pregnancy history; potential markers for lack of menstrual regularity, heavy flow, dysmenorrhea, contraceptives were also identified. Other features such as mood fluctuations and facial speckles could potentially be deduced from the vagino-cervical microbiome. Gut and oral microbiome, plasma vitamins, metals, amino acids and hormones showed associations with the vagino-cervical microbiome. Our results offer an unprecedented glimpse into the microbiota of the female reproductive tract and call for international collaborations to better understand its long-term health impact. Highlights:Shotgun sequencing of 1148 vagino-cervical samples reveal subtypes; 1Other omics such as moods and skin features could be predicted by the vagino-cervical 2 bacteria; 3Factors such as delivery mode and breast-feeding associate with the vagino-cervical 4 microbiome; 5With dwindled Lactobacilli, postmenopausal samples are relatively enriched for viruses. 6 7 3 4 vulvovaginal candidiasis (Bradford and Ravel, 2017). The over 90% of human 30 sequences in female reproductive tract samples, in contrast to 1% in feces (Li et al., 31 2018; Methé et al., 2012; Wang and Jia, 2016), has made metagenomic shotgun 32 sequencing more expensive. Most studies of the vaginal microbiota used 16S rRNA 33 gene amplicon sequencing, which lacked a view of the overall microorganism 34 communities including bacteria, archaea, viruses and fungi (Byrd et al., 2018), as well 35 as the functional capacity encoded. Besides infection, studies on current sexual activity 36 and the menstrual cycle occurred naturally to the vaginal microbiota field (Gajer et al., 37 2012; Ravel et al., 2010). However, lasting impacts from other potentially important 38 factors such as sexual debut, pregnancy and breast-feeding have not been looked at in 39 a reasonably large cohort. 40 41 As a sizable reservoir of microbes instead of a transient entity, the female reproductive 42 tract microbiota might also reflect conditions in other body sites. It is however not clear 43 whether other omics in circulation or in the intestine cross-talks with the vagino-cervical 44 microbiome. Intersecting with hormones, metabolic and immune functions, we find it 45intriguing to explore the potential link of the vagino-cervical microbiome to the brain and 46 the face. 47 5 data, immune indices, physical fitness test, facial skin imaging, as well as female life 53 history questionnaire, lifestyle questionnaire, and psychological questionnaire (Figure 1). 54Our work pinpoints other metadata or omics that can predict or be predicted from the 55 microbiota in the female reproductive tr...

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Visualization of microbes by 16S in situ hybridization in term and preterm placentas without intraamniotic infection

Cited by 100 publications

References 93 publications

Lack of evidence for microbiota in the placental and fetal tissues of rhesus macaques

Lack of evidence for microbiota in the placental and fetal tissues of rhesus macaques

The composition of the perinatal intestinal microbiota in horse

The vagino-cervical microbiome as a woman’s life history

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