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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-06-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00210-20 |
| _version_ | 1818740190446878720 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-18T01:36:47Z |
| format | Article |
| id | doaj.art-b9f28c7369474cd4b2f2ed444456f4ed |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-18T01:36:47Z |
| publishDate | 2020-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-b9f28c7369474cd4b2f2ed444456f4ed2022-12-21T21:25:26ZengAmerican Society for MicrobiologymSphere2379-50422020-06-015310.1128/mSphere.00210-20Lack of Evidence for Microbiota in the Placental and Fetal Tissues of Rhesus MacaquesKevin R. Theis0Roberto Romero1Andrew D. Winters2Alan H. Jobe3Nardhy Gomez-Lopez4Department of Biochemistry, Microbiology and Immunology, Wayne State University School of Medicine, Detroit, Michigan, USAPerinatology Research Branch, Division of Obstetrics and Maternal-Fetal Medicine, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services, Bethesda, Maryland, and Detroit, Michigan, USADepartment of Biochemistry, Microbiology and Immunology, Wayne State University School of Medicine, Detroit, Michigan, USACincinnati Children’s Hospital, University of Cincinnati School of Medicine, Cincinnati, Ohio, USADepartment of Biochemistry, Microbiology and Immunology, Wayne State University School of Medicine, Detroit, Michigan, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mSphere.00210-20microbiomelow microbial biomasspregnancyin utero colonizationnonhuman primate model |
| spellingShingle | 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 mSphere microbiome low microbial biomass pregnancy in utero colonization nonhuman primate model |
| title | 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_short | 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 |
| topic | microbiome low microbial biomass pregnancy in utero colonization nonhuman primate model |
| url | https://journals.asm.org/doi/10.1128/mSphere.00210-20 |
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