Skip to main content
SpringerLink
Log in

Vaginal Microbiota Is Stable and Mainly Dominated by Lactobacillus at Third Trimester of Pregnancy and Active Childbirth: A Longitudinal Study of Ten Mexican Women

  • Short Communication
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

In healthy women at reproductive age, the vaginal microbiota is mainly dominated by Lactobacillus bacteria during pregnancy and non-pregnancy stages. However, little is known about longitudinal changes within the vaginal microbiota composition from the third trimester of pregnancy to childbirth in healthy women. Thus, we conducted an exploratory longitudinal study of vaginal microbiota composition of 10 Mexican pregnant women, sampling from the same volunteer at two-time points: third trimester of pregnancy and active childbirth. Vaginal bacterial microbiota was characterized by V3-16S rDNA libraries by high-throughput sequencing and bioinformatics methods. Out of ten, vaginal microbiota from eight women was dominated by the Lactobacillus genus at both time points, whereas the other two women showed vaginal microbiota composition with high abundance of genera Gardnerella, Prevotella, and members of the Atopobiaceae family, without any preterm birth correlation. Importantly, we found no statistically significant differences in relative abundances, absolute reads count, alpha and beta diversity between the third trimester of pregnancy, and active childbirth time points. However, compared to the third trimester of pregnancy, we observed a trend with higher absolute reads counts for Gardnerella, Faecalibaculum, Ileibacterium, and Lactococcus genus at active childbirth and lower absolute reads count of Lactobacillus genus. Our results suggest that the vaginal microbiota composition is stable, and Lactobacillus genus is the dominant taxa in Mexican women’s vagina at the third trimester of pregnancy and childbirth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data Availability

The sequencing data that support this study were deposited in the NCBI by sequence read archive. The submission number is SUB10006742 and BioProject accession number: PRJNA746573.

Code Availability

The relative microbial abundance at genus taxonomic levels and alpha and beta diversity of the third trimester of pregnancy and childbirth were determined using QIIME2 pipeline [21] and graphics using Phyloseq [23], ggplot2 packages in R environment (v3.4.4).

References

  1. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL et al (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108:4680–4687. https://doi.org/10.1073/pnas.1002611107

    Article  PubMed  Google Scholar 

  2. O’Hanlon DE, Moench TR, Cone RA (2011) In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis. https://doi.org/10.1186/1471-2334-11-200

    Article  PubMed  PubMed Central  Google Scholar 

  3. Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UME, Zhong X et al (2012) Temporal dynamics of the human vaginal microbiota. Sci Transl Med. https://doi.org/10.1126/scitranslmed.3003605

    Article  PubMed  PubMed Central  Google Scholar 

  4. Martin DH (2012) The microbiota of the vagina and its influence on women’s health and disease. Am J Med Sci 343:2–9. https://doi.org/10.1097/MAJ.0b013e31823ea228

    Article  PubMed  PubMed Central  Google Scholar 

  5. DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A et al (2015) Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A 112:11060–11065. https://doi.org/10.1073/pnas.1502875112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Meis PJ, Michielutte R, Peters TJ, Wells HB, Sands RE, Coles EC et al (1995) Factors associated with preterm birth in Cardiff, Wales: II. Indicated and spontaneous preterm birth. Am J Obstet Gynecol 173:597–602. https://doi.org/10.1016/0002-9378(95)90288-0

    Article  CAS  PubMed  Google Scholar 

  7. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF, Petraglia F (2009) Inflammation and pregnancy. Reprod Sci 16:206–215. https://doi.org/10.1177/1933719108329095

    Article  CAS  PubMed  Google Scholar 

  8. Siiteri PK, MacDonald PC (1966) Placental estrogen biosynthesis during human pregnancy. J Clin Endocrinol Metab 26:751–761. https://doi.org/10.1210/jcem-26-7-751

    Article  CAS  PubMed  Google Scholar 

  9. O’Hanlon DE, Moench TR, Cone RA (2013) Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS ONE 8:1–8. https://doi.org/10.1371/journal.pone.0080074

    Article  CAS  Google Scholar 

  10. Walther-António MRS, Jeraldo P, Berg Miller ME, Yeoman CJ, Nelson KE, Wilson BA et al (2014) Pregnancy’s stronghold on the vaginal microbiome. PLoS ONE 9:1–10. https://doi.org/10.1371/journal.pone.0098514

    Article  CAS  Google Scholar 

  11. Serrano MG, Parikh HI, Brooks JP, Edwards DJ, Arodz TJ, Edupuganti L et al (2019) Racioethnic diversity in the dynamics of the vaginal microbiome during pregnancy. Nat Med 25:1001–1011. https://doi.org/10.1038/s41591-019-0465-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fettweis JM, Paul Brooks J, Serrano MG, Sheth NU, Girerd PH, Edwards DJ et al (2014) Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiol (United Kingdom) 160:2272–2282. https://doi.org/10.1099/mic.0.081034-0

    Article  CAS  Google Scholar 

  13. Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P et al (2007) Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 1:121–133. https://doi.org/10.1038/ismej.2007.12

    Article  CAS  PubMed  Google Scholar 

  14. Vargas-Robles D, Morales N, Rodríguez I, Nieves T, Godoy-Vitorino F, Alcaraz LD et al (2020) Changes in the vaginal microbiota across a gradient of urbanization. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-69111-x

    Article  CAS  Google Scholar 

  15. Hernández-Rodríguez C, Romero-González R, Albani-Campanario M, Figueroa-Damián R, Meraz-Cruz N, Hernández-Guerrero C (2011) Vaginal microbiota of healthy pregnant Mexican women is constituted by four lactobacillus species and several vaginosis-associated bacteria. Infect Dis Obstet Gynecol. https://doi.org/10.1155/2011/851485

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hinckley AF, Bachand AM, Reif JS (2005) Late pregnancy exposures to disinfection by-products and growth-related birth outcomes. Environ Health Perspect 113:1808–1813. https://doi.org/10.1289/ehp.8282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Reyes-Lagos JJ, Echeverría-Arjonilla JC, Peña-Castillo MÁ, Montiel-Castro AJ, Pacheco-López G (2014) Physiological, immunological and evolutionary perspectives of labor as an inflammatory process. Adv Neuroimmune Biol 5:75–89. https://doi.org/10.3233/NIB-140085

    Article  Google Scholar 

  18. Nirmalkar K, Murugesan S, Pizano-Zárate ML, Villalobos-Flores LE, García-González C, Morales-Hernández RM et al (2018) Gut microbiota and endothelial dysfunction markers in obese Mexican children and adolescents. Nutrients. https://doi.org/10.3390/nu10122009

    Article  PubMed  PubMed Central  Google Scholar 

  19. García-Mena J, Murugesan S, Pérez-Muñoz AA, García-Espitia M, Maya O, Jacinto-Montiel M et al (2016) Airborne bacterial diversity from the low atmosphere of greater Mexico City. Microb Ecol 72:70–84. https://doi.org/10.1007/s00248-016-0747-3

    Article  CAS  PubMed  Google Scholar 

  20. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P et al (2013) The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  Google Scholar 

  23. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. https://doi.org/10.1371/journal.pone.0061217

    Article  PubMed  PubMed Central  Google Scholar 

  24. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  25. Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM et al (2019) PICRUSt2: an improved and extensible approach for metagenome inference. bioRxiv. https://doi.org/10.1101/672295

    Article  Google Scholar 

  26. Reyes-Lagos JJ, Peña-Castillo MÁ, Echeverría JC, Pérez-Sánchez G, Álvarez-Herrera S, Becerril-Villanueva E et al (2017) Women serum concentrations of the IL-10 family of cytokines and IFN-γ decrease from the third trimester of pregnancy to active labor. NeuroImmunoModulation 24:162–170. https://doi.org/10.1159/000480734

    Article  CAS  PubMed  Google Scholar 

  27. Nunn KL, Witkin SS, Schneider GM, Boester A, Nasioudis D, Minis E et al (2021) Changes in the vaginal microbiome during the pregnancy to postpartum transition. Reprod Sci. https://doi.org/10.1007/s43032-020-00438-6

    Article  PubMed  Google Scholar 

  28. Avershina E, Slangsvold S, Simpson MR, Storrø O, Johnsen R, Øien T et al (2017) Diversity of vaginal microbiota increases by the time of labor onset. Sci Rep 7:1–7. https://doi.org/10.1038/s41598-017-17972-0

    Article  CAS  Google Scholar 

  29. Li L, Qin Y, Kong Z, Wu J, Kubota K, Li YY (2019) Characterization of microbial community and main functional groups of prokaryotes in thermophilic anaerobic co-digestion of food waste and paper waste. Sci Total Environ 652:709–717. https://doi.org/10.1016/j.scitotenv.2018.10.292

    Article  CAS  PubMed  Google Scholar 

  30. Aldunate M, Srbinovski D, Hearps AC, Latham CF, Ramsland PA, Gugasyan R et al (2015) Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis. Front Physiol 6:1–23. https://doi.org/10.3389/fphys.2015.00164

    Article  Google Scholar 

  31. Westerholm M, Liu T, Schnürer A (2020) Comparative study of industrial-scale high-solid biogas production from food waste: process operation and microbiology. Bioresour Technol 304:122981. https://doi.org/10.1016/j.biortech.2020.122981

    Article  CAS  PubMed  Google Scholar 

  32. Zheng D, Wang HZ, Gou M, Nobu MK, Narihiro T, Hu B et al (2019) Identification of novel potential acetate-oxidizing bacteria in thermophilic methanogenic chemostats by DNA stable isotope probing. Appl Microbiol Biotechnol 103:8631–8645. https://doi.org/10.1007/s00253-019-10078-9

    Article  CAS  PubMed  Google Scholar 

  33. Timmers PHA, Vavourakis CD, Kleerebezem R, Sinninghe Damsté JS, Muyzer G, Stams AJM et al (2018) Metabolism and occurrence of methanogenic and sulfate-reducing syntrophic acetate oxidizing communities in haloalkaline environments. Front Microbiol 9:1–18. https://doi.org/10.3389/fmicb.2018.03039

    Article  Google Scholar 

  34. Sasaki K, Morita M, Hirano SI, Ohmura N, Igarashi Y (2011) Decreasing ammonia inhibition in thermophilic methanogenic bioreactors using carbon fiber textiles. Appl Microbiol Biotechnol 90:1555–1561. https://doi.org/10.1007/s00253-011-3215-5

    Article  CAS  PubMed  Google Scholar 

  35. Zhu X, Kougias PG, Treu L, Campanaro S, Angelidaki I (2017) Microbial community changes in methanogenic granules during the transition from mesophilic to thermophilic conditions. Appl Microbiol Biotechnol 101:1313–1322. https://doi.org/10.1007/s00253-016-8028-0

    Article  CAS  PubMed  Google Scholar 

  36. Zhao J, Westerholm M, Qiao W, Yin D, Bi S, Jiang M et al (2018) Impact of temperature and substrate concentration on degradation rates of acetate, propionate and hydrogen and their links to microbial community structure. Bioresour Technol 256:44–52. https://doi.org/10.1016/J.BIORTECH.2018.01.150

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Alberto Piña-Escobedo (Cinvestav) for Ion Torrent semiconductor DNA sequencing. JG-M (19815), GP-L (89770), JJR-L (381983), MAP-C (61855), and AG-S (513607) are Fellows of the Sistema Nacional de Investigadores, Mexico.

Funding

This research was partially funded by CONACyT Grant Number INFR-2011-1-163235 (JG-M), CB-2015 255399 to GP-L, and Universidad Autónoma Metropolitana (UAM) institutional fund to GP-L.

Author information

Author notes

  1. Khemlal Nirmalkar

    Present address: Biodesign Center for Health Through Microbiomes, Arizona State University, Tempe, AZ, USA

Authors and Affiliations

  1. Biological and Health Sciences Division, Metropolitan Autonomous University (UAM), Campus Lerma, Lerma, Mexico

    Antonio González-Sánchez & Gustavo Pacheco-López

  2. School of Medicine, Autonomous University of Mexico State (UAEMex), Toluca, Mexico

    José J. Reyes-Lagos

  3. Basic Sciences and Engineering Division, Metropolitan Autonomous University (UAM), Campus Iztapalapa, Mexico City, Mexico

    Miguel A. Peña-Castillo

  4. Genetic and Molecular Biology Department, Center of Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), Campus Zacatenco, Mexico City, Mexico

    Khemlal Nirmalkar & Jaime García-Mena

Authors
  1. Antonio González-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José J. Reyes-Lagos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miguel A. Peña-Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Khemlal Nirmalkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jaime García-Mena
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gustavo Pacheco-López
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, review, and editing, all authors; Data curation, AGS and KN; Vaginal swab collection, JJRL and MAPC; Resources and founding acquisition, GPL and JGM; Writing, all authors; All authors read, review and approved the final manuscript.

Corresponding authors

Correspondence to Jaime García-Mena or Gustavo Pacheco-López.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical Approval

The research protocol was approved by the Ethics Committee from the Biological and Health Sciences Division (CBS) at the Metropolitan Autonomous University (UAM), Campus Iztapalapa (Ref. CAEDCBS.01.2017), and informed consent was obtained from each participant. This study was conducted following the Declaration of Helsinki and the institutional procedures of Maternal and Childhood Research Center (CIMIGen) and UAM.

Consent to Participate

Informed consent was obtained from all participants included in the study.

Consent to Publication

The participant has consented to submit of the case report to the journal.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Sánchez, A., Reyes-Lagos, J.J., Peña-Castillo, M.A. et al. Vaginal Microbiota Is Stable and Mainly Dominated by Lactobacillus at Third Trimester of Pregnancy and Active Childbirth: A Longitudinal Study of Ten Mexican Women. Curr Microbiol 79, 230 (2022). https://doi.org/10.1007/s00284-022-02918-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-022-02918-1

Search

Navigation