Skip to main content

Probiotic supplements alleviate gestational diabetes mellitus by restoring the diversity of gut microbiota: a study based on 16S rRNA sequencing

Journal of Microbiology volume 59, pages 827–839 (2021)Cite this article

Abstract

Probiotics effectively prevent and improve metabolic diseases such as diabetes by regulating the intestinal microenvironment and gut microbiota. However, the effects of probiotics in gestational diabetes mellitus are not clear. Here, we showed that probiotic supplements significantly improved fasting blood glucose in a gestational diabetes mellitus rat model. To further understand the mechanisms of probiotics in gestational diabetes mellitus, the gut microbiota were analyzed via 16S rRNA sequencing. We found that compared with the normal pregnant group, the gestational diabetes mellitus rats had decreased diversity of gut microbiota. Moreover, probiotic supplementation restored the diversity of the gut microbiota in gestational diabetes mellitus rats, and the gut microbiota structure tended to be similar to that of normal pregnant rats. In particular, compared with gestational diabetes mellitus rats, the abundance of Firmicutes and Actinobacteria was higher after probiotic supplementation. Furthermore, activating carbohydrate metabolism and membrane transport pathways may be involved in the potential mechanisms by which probiotic supplements alleviate gestational diabetes mellitus. Overall, our results suggested that probiotic supplementation might be a novel approach to restore the gut microbiota of gestational diabetes mellitus rats and provided an experimental evidence for the use of probiotic supplements to treat gestational diabetes mellitus.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Abdollahi, M., Farzaei, M.H., Rahimi, R., and Farzaei, F. 2015. Traditional medicinal herbs for the management of diabetes and its complications: an evidence-based review. Int. J. Pharmacol. 11, 874–887.

    Article  CAS  Google Scholar 

  • Adler, C.J., Dobney, K., Weyrich, L.S., Kaidonis, J., Walker, A.W., Haak, W., Bradshaw, C.J.A., Townsend, G., Sołtysiak, A., Kurt, W.A., et al. 2013. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat. Genet. 45, 450–455.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Al-Ajlan, A., Al-Musharaf, S., Fouda, M.A., Krishnaswamy, S., Wani, K., Aljohani, N.J., Al-Serehi, A., Sheshah, E., Alshingetti, N.M., Turkistani, I.Z., et al. 2018. Lower vitamin D levels in Saudi pregnant women are associated with higher risk of developing GDM. BMC Pregnancy Childbirth 18, 86.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Andreasen, A.S., Larsen, N., Pedersen-Skovsgaard, T., Berg, R.M.G., Møller, K., Svendsen, K.D., Jakobsen, M., and Pedersen, B.K. 2010. Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br. J. Nutr. 104, 1831–1838.

    CAS  PubMed  Article  Google Scholar 

  • Bellamy, L., Casas, J., Hingorani, A.D., and Williams, D. 2009. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet 373, 1773–1779.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bolger, A.M., Lohse, M., and Usadel, B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Buchanan, T.A., Xiang, A.H., and Page, K.A. 2012. Gestational diabetes mellitus: risks and management during and after pregnancy. Nat. Rev. Endocrinol. 8, 639–649.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Camarinha-Silva, A., Jáuregui, R., Chaves-Moreno, D., Oxley, A.P.A., Schaumburg, F., Becker, K., Wos-Oxley, M.L., and Pieper, D.H. 2014. Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ. Microbiol. 16, 2939–2952.

    CAS  PubMed  Article  Google Scholar 

  • Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Catalano, P.M., McIntyre, H.D., Cruickshank, J.K., McCance, D.R., Dyer, A.R., Metzger, B.E., Lowe, L.P., Trimble, E.R., Coustan, D.R., Hadden, D.R., et al. 2012. The hyperglycemia and adverse pregnancy outcome study: associations of GDM and obesity with pregnancy outcomes. Diabetes Care 35, 780–786.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Douglas, G.M., Maffei, V.J., Zaneveld, J.R., Yurgel, S.N., Brown, J.R., Taylor, C.M., Huttenhower, C., and Langille, C.I. 2020. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Du, M.K. 2017. PLAC1 related to gestational diabetes. Ph.D. thesis. Zhejiang University, Hangzhou, Zhejiang, P. R. China.

    Google Scholar 

  • Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Fåk, F., Ahrné, S., Molin, G., Jeppsson, B., and Weström, B. 2008. Maternal consumption of Lactobacillus plantarum 299v affects gastrointestinal growth and function in the suckling rat. Br. J. Nutr. 100, 332–338.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Ferrocino, I., Ponzo, V., Gambino, R., Zarovska, A., Leone, F., Monzeglio, C., Goitre, I., Rosato, R., Romano, R., Grassi, G., et al. 2018. Changes in the gut microbiota composition during pregnancy in patients with gestational diabetes mellitus (GDM). Sci. Rep. 8, 12216.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Hasan, S., Aho, V., Pereira, P., Paulin, L., Koivusalo, S.B., Auvinen, P., and Eriksson, J.G. 2018. Gut microbiome in gestational diabetes: a cross-sectional study of mothers and offspring 5 years post-partum. Acta Obstet. Gynecol. Scand. 97, 38–46.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Hsieh, F.C., Lee, C.L., Chai, C.Y., Chen, W.T., Lu, Y.C., and Wu, C.S. 2013. Oral administration of Lactobacillusreuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutr. Metab. 10, 35.

    CAS  Article  Google Scholar 

  • Hu, F., Niu, Y., Xu, X., Hu, Q., Su, Q., and Zhang, H. 2020. Resistant dextrin improves high-fat-high fructose diet induced insulin resistance. Nutr. Metab. 17, 36.

    Article  CAS  Google Scholar 

  • Hu, J., Nomura, Y., Bashir, A., Fernandez-Hernandez, H., Itzkowitz, S., Pei, Z., Stone, J., Loudon, H., and Peter, I. 2013. Diversified microbiota of meconium is affected by maternal diabetes status. PLoS ONE 8, e78257.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Huang, H.Y., Korivi, M., Tsai, C.H., Yang, J.H., and Tsai, Y.C. 2013. Supplementation of Lactobacillus plantarum K68 and fruit-vegetable ferment along with high fat-fructose diet attenuates metabolic syndrome in rats with insulin resistance. Evid. Based Complement Alternat. Med. 2013, 943020.

    PubMed  PubMed Central  Google Scholar 

  • Huang, Q.T., Zhou, L., and Zhong, M. 2017. Advances in the study of the correlation between intestinal flora and probiotics and complications during pregnancy. Obstet. Gynecol. Genet. 7, 56–60. doi: https://doi.org/10.3868/j.issn.2095-1558.2017.01.013.

    Google Scholar 

  • International Diabetes Federation. 2017. IDF Diabetes atlas. 8th edn. International Diabetes Federation. Brussels, Belgium. ISBN: 978-2-930229-87-4.

    Google Scholar 

  • Jia, L., Li, D., Feng, N., Shamoon, M., Sun, Z., Ding, L., Zhang, H., Chen, W., Sun, J., and Chen, Y.Q. 2017. Anti-diabetic effects of Clostridium butyricum CGMCC0313.1 through promoting the growth of gut butyrate-producing bacteria in type 2 diabetic mice. Sci. Rep. 7, 7046.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Langille, M.G.I., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Thurber, R.L.V., Knight, R., et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Leng, J., Shao, P., Zhang, C., Tian, H., Zhang, F., Zhang, S., Dong, L., Li, L., Yu, Z., Chan, J.C.N., et al. 2015. Prevalence of gestational diabetes mellitus and its risk factors in Chinese pregnant women: a prospective population-based study in Tianjin, China. PLoS ONE 10, e0121029.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Li, X., Huang, Y., Song, L., Xiao, Y., Lu, S., Xu, J., Li, J., and Ren, Z. 2020. Lactobacillus plantarum prevents obesity via modulation of gut microbiota and metabolites in high-fat feeding mice. J. Funct. Foods 73, 104103.

    CAS  Article  Google Scholar 

  • Lv, S., Liu, H., Pan, L., Sun, J., and Lu, Z. 2018. Advances in the study on changes of intestinal flora and probiotics during pregnancy. J. Pract. Med. 34, 3849–3853. doi: https://doi.org/10.3969/j.issn.1006-5725.2018.23.004.

    Google Scholar 

  • Magoč, T. and Salzberg, S.L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Nitert, M.D., Barrett, H.L., Foxcroft, K., Tremellen, A., Wilkinson, S., Lingwood, B., Tobin, J.M., McSweeney, C., O’Rourke, P., McIntyre, H.D., et al. 2013. SPRING: an RCT study of probiotics in the prevention of gestational diabetes mellitus in overweight and obese women. BMC Pregnancy Childbirth 13, 50.

    PubMed  PubMed Central  Article  Google Scholar 

  • Park, S.S., Lee, Y.J., Kang, H., Yang, G., Hong, E.J., Lim, J.Y., Oh, S., and Kim, E. 2019. Lactobacillus amylovorus KU4 ameliorates diet-induced obesity in mice by promoting adipose browning through PPARγ signaling. Sci. Rep. 9, 20152.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Simon, M.C., Strassburger, K., Nowotny, B., Kolb, H., Nowotny, P., Burkart, V., Zivehe, F., Hwang, J.H., Stehle, P., Pacini, G., et al. 2015. Intake of Lactobacillus reuteri improves incretin and insulin secretion in glucose tolerant humans: a proof of concept. Diabetes Care 38, 1827–1834.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Su, M., Nie, Y., Shao, R., Duan, S., Jiang, Y., Wang, M., Xing, Z., Sun, Q., Liu, X., and Xu, W. 2018. Diversified gut microbiota in new-borns of mothers with gestational diabetes mellitus. PLoS ONE 13, e0205695.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., et al. 2009. A core gut microbiome in obese and lean twins. Nature 457, 480–484.

    CAS  PubMed  Article  Google Scholar 

  • Tzounis, X., Rodriguez-Mateos, A., Vulevic, J., Gibson, G.R., Kwik-Uribe, C., and Spencer, J.P. 2011. Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am. J. Clin. Nutr. 93, 62–72.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Veeraswamy, S., Vijayam, B., Gupta, V.K., and Kapur, A. 2012. Gestational diabetes: the public health relevance and approach. Diabetes Res. Clin. Pract. 97, 350–358.

    PubMed  Article  Google Scholar 

  • Wang, Y., Sheng, H.F., He, Y., Wu, J.Y., Jiang, Y.X., Tam, N.F.Y., and Zhou, H.W. 2012. Comparison of the levels of bacterial diversity in fresh water, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl. Environ. Microbiol. 78, 8264–8271.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yan, F., Li, N., Shi, J., Li, H., Yue, Y., Jiao, W., Wang, N., Song, Y., Huo, G., and Li, B. 2019. Lactobacillus acidophilus alleviates type 2 diabetes by regulating hepatic glucose, lipid metabolism and gut microbiota in mice. Food Funct. 10, 5804–5815.

    CAS  PubMed  Article  Google Scholar 

  • Ye, G., Zhang, L., Wang, M., Chen, Y., Gu, S., Wang, K., Leng, J., Gu, Y., and Xie, Y. 2019. The gut microbiota in women suffering from gestational diabetes mellitus with the failure of glycemic control by lifestyle modification. J. Diabetes Res. 2019, 6081248.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zhang, L., Luo, J., Li, X., Guo, S., and Shi, D. 2020. 16S rRNA sequencing and metagenomics study of gut microbiota: implications of BDB on type 2 diabetes mellitus. Mar. Drugs 18, 469.

    CAS  PubMed Central  Article  Google Scholar 

  • Zhang, C., Wang, W., He, Q., and Hu, P. 2017. Analysis of the characteristics of important intestinal flora in gestational diabetes mellitus and its correlation with inflammatory factors. Chin. J. Diabetes 25, 320–324.

    Google Scholar 

  • Zheng, X., Shen, X., Zhang, Z., Liu, Y., Dong, Z., and Chen B. 2018. Advances in the study of probiotics in the regulation of blood glucose. Chin. J. Microecol. 30, 222–228.

    Google Scholar 

Download references

Acknowledgements

This work has been supported by by a grant from Fujian Maternity and Child Health Hospital (YCXMH 20-08).

Author information

Affiliations

  1. Fujian Maternity and Child Health Hospital Affiliated to Fujian Medical University, Fuzhou, 350000, P. R. China

    Qing-Xiang Zheng, Xiu-Min Jiang & Hai-Wei Wang

  2. Fujian University of Traditional Chinese Medicine, Fuzhou, 350122, P. R. China

    Li Ge, Yu-Ting Lai, Xin-Yong Jiang, Fan Chen & Ping-Ping Huang

Authors
  1. Qing-Xiang Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiu-Min Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hai-Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu-Ting Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xin-Yong Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ping-Ping Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiu-Min Jiang.

Additional information

Conflict of Interest

The authors declare that they have no competing interests.

Ethical Statement

All animal procedures were approved and conducted under the guidance of the animal experiment center at Fujian University of Traditional Chinese Medicine. Animal ethics approval number was FJTCM IACUC 2020020.

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zheng, QX., Jiang, XM., Wang, HW. et al. Probiotic supplements alleviate gestational diabetes mellitus by restoring the diversity of gut microbiota: a study based on 16S rRNA sequencing. J Microbiol. 59, 827–839 (2021). https://doi.org/10.1007/s12275-021-1094-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-021-1094-8

Keywords

  • gut microbiota
  • probiotics
  • gestational diabetes mellitus
  • 16S rRNA sequencing