Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques

ABSTRACT The 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 whether the fetal and placental tissues of rhesus macaq...

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Autores principales:	Kevin R. Theis, Roberto Romero, Andrew D. Winters, Alan H. Jobe, Nardhy Gomez-Lopez
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	microbiome low microbial biomass pregnancy in utero colonization nonhuman primate model Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b9f28c7369474cd4b2f2ed444456f4ed
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spelling	oai:doaj.org-article:b9f28c7369474cd4b2f2ed444456f4ed2021-11-15T15:30:15ZLack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques10.1128/mSphere.00210-202379-5042https://doaj.org/article/b9f28c7369474cd4b2f2ed444456f4ed2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00210-20https://doaj.org/toc/2379-5042ABSTRACT The 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 whether the fetal and placental tissues of rhesus macaques harbor bacterial communities. Fetal, placental, and uterine wall samples were obtained from cesarean deliveries without labor (∼130/166 days gestation). The presence of bacteria in the fetal intestine and placenta was investigated through culture. The bacterial burden and profiles 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 profiles of fetal and placental tissues did not exceed or differ from those of background technical controls. By 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 bacterial communities in the fetal and placental tissues of rhesus macaques. IMPORTANCE Microbial 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 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 and 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, quantitative real-time PCR [qPCR], and DNA sequencing) and controlling for potential background DNA contamination, we did not find consistent evidence for microbial communities in the placental and fetal tissues of rhesus macaques.Kevin R. TheisRoberto RomeroAndrew D. WintersAlan H. JobeNardhy Gomez-LopezAmerican Society for Microbiologyarticlemicrobiomelow microbial biomasspregnancyin utero colonizationnonhuman primate modelMicrobiologyQR1-502ENmSphere, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	microbiome low microbial biomass pregnancy in utero colonization nonhuman primate model Microbiology QR1-502
spellingShingle	microbiome low microbial biomass pregnancy in utero colonization nonhuman primate model Microbiology QR1-502 Kevin R. Theis Roberto Romero Andrew D. Winters Alan H. Jobe Nardhy Gomez-Lopez Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques
description	ABSTRACT The 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 whether the fetal and placental tissues of rhesus macaques harbor bacterial communities. Fetal, placental, and uterine wall samples were obtained from cesarean deliveries without labor (∼130/166 days gestation). The presence of bacteria in the fetal intestine and placenta was investigated through culture. The bacterial burden and profiles 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 profiles of fetal and placental tissues did not exceed or differ from those of background technical controls. By 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 bacterial communities in the fetal and placental tissues of rhesus macaques. IMPORTANCE Microbial 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 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 and 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, quantitative real-time PCR [qPCR], and DNA sequencing) and controlling for potential background DNA contamination, we did not find consistent evidence for microbial communities in the placental and fetal tissues of rhesus macaques.
format	article
author	Kevin R. Theis Roberto Romero Andrew D. Winters Alan H. Jobe Nardhy Gomez-Lopez
author_facet	Kevin R. Theis Roberto Romero Andrew D. Winters Alan H. Jobe Nardhy Gomez-Lopez
author_sort	Kevin R. Theis
title	Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques
title_short	Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques
title_full	Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques
title_fullStr	Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques
title_full_unstemmed	Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques
title_sort	lack of evidence for microbiota in the placental and fetal tissues of rhesus macaques
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/b9f28c7369474cd4b2f2ed444456f4ed
work_keys_str_mv	AT kevinrtheis lackofevidenceformicrobiotaintheplacentalandfetaltissuesofrhesusmacaques AT robertoromero lackofevidenceformicrobiotaintheplacentalandfetaltissuesofrhesusmacaques AT andrewdwinters lackofevidenceformicrobiotaintheplacentalandfetaltissuesofrhesusmacaques AT alanhjobe lackofevidenceformicrobiotaintheplacentalandfetaltissuesofrhesusmacaques AT nardhygomezlopez lackofevidenceformicrobiotaintheplacentalandfetaltissuesofrhesusmacaques
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Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus Macaques

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