Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies

A comparative analysis of the placental microbiome in pregnancies with late fetal growth restriction (FGR) was performed with normal pregnancies to assess the impact of bacteria on placental development and function. The presence of microorganisms in the placenta, amniotic fluid, fetal membranes and...

Full description

Bibliographic Details
Main Authors: Aleksandra Stupak, Tomasz Gęca, Anna Kwaśniewska, Radosław Mlak, Paweł Piwowarczyk, Robert Nawrot, Anna Goździcka-Józefiak, Wojciech Kwaśniewski
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/8/6922
_version_ 1797605143685890048
author Aleksandra Stupak
Tomasz Gęca
Anna Kwaśniewska
Radosław Mlak
Paweł Piwowarczyk
Robert Nawrot
Anna Goździcka-Józefiak
Wojciech Kwaśniewski
author_facet Aleksandra Stupak
Tomasz Gęca
Anna Kwaśniewska
Radosław Mlak
Paweł Piwowarczyk
Robert Nawrot
Anna Goździcka-Józefiak
Wojciech Kwaśniewski
author_sort Aleksandra Stupak
collection DOAJ
description A comparative analysis of the placental microbiome in pregnancies with late fetal growth restriction (FGR) was performed with normal pregnancies to assess the impact of bacteria on placental development and function. The presence of microorganisms in the placenta, amniotic fluid, fetal membranes and umbilical cord blood throughout pregnancy disproves the theory of the “sterile uterus”. FGR occurs when the fetus is unable to follow a biophysically determined growth path. Bacterial infections have been linked to maternal overproduction of pro-inflammatory cytokines, as well as various short- and long-term problems. Proteomics and bioinformatics studies of placental biomass allowed the development of new diagnostic options. In this study, the microbiome of normal and FGR placentas was analyzed by LC-ESI-MS/MS mass spectrometry, and the bacteria present in both placentas were identified by analysis of a set of bacterial proteins. Thirty-six pregnant Caucasian women participated in the study, including 18 women with normal pregnancy and eutrophic fetuses (EFW > 10th percentile) and 18 women with late FGR diagnosed after 32 weeks of gestation. Based on the analysis of the proteinogram, 166 bacterial proteins were detected in the material taken from the placentas in the study group. Of these, 21 proteins had an exponentially modified protein abundance index (emPAI) value of 0 and were not included in further analysis. Of the remaining 145 proteins, 52 were also present in the material from the control group. The remaining 93 proteins were present only in the material collected from the study group. Based on the proteinogram analysis, 732 bacterial proteins were detected in the material taken from the control group. Of these, 104 proteins had an emPAI value of 0 and were not included in further analysis. Of the remaining 628 proteins, 52 were also present in the material from the study group. The remaining 576 proteins were present only in the material taken from the control group. In both groups, we considered the result of ns prot ≥ 60 as the cut-off value for the agreement of the detected protein with its theoretical counterpart. Our study found significantly higher emPAI values of proteins representative of the following bacteria: <i>Actinopolyspora erythraea</i>, <i>Listeria costaricensis</i>, <i>E. coli</i>, <i>Methylobacterium</i>, <i>Acidobacteria bacterium</i>, <i>Bacteroidetes bacterium</i>, <i>Paenisporsarcina</i> sp., <i>Thiodiazotropha endol oripes</i> and <i>Clostridiales bacterium</i>. On the other hand, in the control group statistically more frequently, based on proteomic data, the following were found: <i>Flavobacterial bacterium</i>, <i>Aureimonas</i> sp. and <i>Bacillus cereus</i>. Our study showed that placental dysbiosis may be an important factor in the etiology of FGR. The presence of numerous bacterial proteins present in the control material may indicate their protective role, while the presence of bacterial proteins detected only in the material taken from the placentas of the study group may indicate their potentially pathogenic nature. This phenomenon is probably important in the development of the immune system in early life, and the placental microbiota and its metabolites may have great potential in the screening, prevention, diagnosis and treatment of FGR.
first_indexed 2024-03-11T04:56:59Z
format Article
id doaj.art-4c9411f6ba734114a42c37f79e69f454
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-11T04:56:59Z
publishDate 2023-04-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-4c9411f6ba734114a42c37f79e69f4542023-11-17T19:32:29ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-04-01248692210.3390/ijms24086922Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological PregnanciesAleksandra Stupak0Tomasz Gęca1Anna Kwaśniewska2Radosław Mlak3Paweł Piwowarczyk4Robert Nawrot5Anna Goździcka-Józefiak6Wojciech Kwaśniewski7Chair and Department of Obstetrics and Pathology of Pregnancy, Medical University of Lublin, 20-059 Lublin, PolandChair and Department of Obstetrics and Pathology of Pregnancy, Medical University of Lublin, 20-059 Lublin, PolandChair and Department of Obstetrics and Pathology of Pregnancy, Medical University of Lublin, 20-059 Lublin, PolandBody Composition Research Laboratory, Department of Preclinical Science, Medical University of Lublin, 20-059 Lublin, Poland2nd Department of Anesthesiology and Intensive Care Unit, Medical University of Lublin, 20-059 Lublin, PolandDepartment of Molecular Virology, Institute of Experimental Biology, Adam Mickiewicz University in Poznan, 61-712 Poznań, PolandDepartment of Molecular Virology, Institute of Experimental Biology, Adam Mickiewicz University in Poznan, 61-712 Poznań, PolandDepartment of Gynecologic Oncology and Gynecology, Medical University of Lublin, 20-059 Lublin, PolandA comparative analysis of the placental microbiome in pregnancies with late fetal growth restriction (FGR) was performed with normal pregnancies to assess the impact of bacteria on placental development and function. The presence of microorganisms in the placenta, amniotic fluid, fetal membranes and umbilical cord blood throughout pregnancy disproves the theory of the “sterile uterus”. FGR occurs when the fetus is unable to follow a biophysically determined growth path. Bacterial infections have been linked to maternal overproduction of pro-inflammatory cytokines, as well as various short- and long-term problems. Proteomics and bioinformatics studies of placental biomass allowed the development of new diagnostic options. In this study, the microbiome of normal and FGR placentas was analyzed by LC-ESI-MS/MS mass spectrometry, and the bacteria present in both placentas were identified by analysis of a set of bacterial proteins. Thirty-six pregnant Caucasian women participated in the study, including 18 women with normal pregnancy and eutrophic fetuses (EFW > 10th percentile) and 18 women with late FGR diagnosed after 32 weeks of gestation. Based on the analysis of the proteinogram, 166 bacterial proteins were detected in the material taken from the placentas in the study group. Of these, 21 proteins had an exponentially modified protein abundance index (emPAI) value of 0 and were not included in further analysis. Of the remaining 145 proteins, 52 were also present in the material from the control group. The remaining 93 proteins were present only in the material collected from the study group. Based on the proteinogram analysis, 732 bacterial proteins were detected in the material taken from the control group. Of these, 104 proteins had an emPAI value of 0 and were not included in further analysis. Of the remaining 628 proteins, 52 were also present in the material from the study group. The remaining 576 proteins were present only in the material taken from the control group. In both groups, we considered the result of ns prot ≥ 60 as the cut-off value for the agreement of the detected protein with its theoretical counterpart. Our study found significantly higher emPAI values of proteins representative of the following bacteria: <i>Actinopolyspora erythraea</i>, <i>Listeria costaricensis</i>, <i>E. coli</i>, <i>Methylobacterium</i>, <i>Acidobacteria bacterium</i>, <i>Bacteroidetes bacterium</i>, <i>Paenisporsarcina</i> sp., <i>Thiodiazotropha endol oripes</i> and <i>Clostridiales bacterium</i>. On the other hand, in the control group statistically more frequently, based on proteomic data, the following were found: <i>Flavobacterial bacterium</i>, <i>Aureimonas</i> sp. and <i>Bacillus cereus</i>. Our study showed that placental dysbiosis may be an important factor in the etiology of FGR. The presence of numerous bacterial proteins present in the control material may indicate their protective role, while the presence of bacterial proteins detected only in the material taken from the placentas of the study group may indicate their potentially pathogenic nature. This phenomenon is probably important in the development of the immune system in early life, and the placental microbiota and its metabolites may have great potential in the screening, prevention, diagnosis and treatment of FGR.https://www.mdpi.com/1422-0067/24/8/6922microbiomebacteriaproteomepregnancyFGRplacenta
spellingShingle Aleksandra Stupak
Tomasz Gęca
Anna Kwaśniewska
Radosław Mlak
Paweł Piwowarczyk
Robert Nawrot
Anna Goździcka-Józefiak
Wojciech Kwaśniewski
Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies
International Journal of Molecular Sciences
microbiome
bacteria
proteome
pregnancy
FGR
placenta
title Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies
title_full Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies
title_fullStr Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies
title_full_unstemmed Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies
title_short Comparative Analysis of the Placental Microbiome in Pregnancies with Late Fetal Growth Restriction versus Physiological Pregnancies
title_sort comparative analysis of the placental microbiome in pregnancies with late fetal growth restriction versus physiological pregnancies
topic microbiome
bacteria
proteome
pregnancy
FGR
placenta
url https://www.mdpi.com/1422-0067/24/8/6922
work_keys_str_mv AT aleksandrastupak comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT tomaszgeca comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT annakwasniewska comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT radosławmlak comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT pawełpiwowarczyk comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT robertnawrot comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT annagozdzickajozefiak comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies
AT wojciechkwasniewski comparativeanalysisoftheplacentalmicrobiomeinpregnancieswithlatefetalgrowthrestrictionversusphysiologicalpregnancies