한국발생생물학회지:발생과생식 (Development and Reproduction)

  • 제26권4호
  • /
  • Pages.145-153
  • /
  • 2022
  • /
  • 2465-9525(pISSN)
  • /
  • 2465-9541(eISSN)
한국발생생물학회 (The Korean Society of Developmental Biology)
권호 표지
DOI QR코드

DOI QR Code

Effects of Antibiotics on the Uterine Microbial Community of Mice

  • Sang-Gyu Kim (Division of Life Sciences, Jeonbuk National University) ;
  • Dae-Wi Kim (Division of Life Sciences, Jeonbuk National University) ;
  • Hoon Jang (Division of Life Sciences, Jeonbuk National University)
  • 투고 : 2022.09.03
  • 심사 : 2022.11.24
  • 발행 : 2022.12.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

The gut microbiota is involved in the maintenance of physiological homeostasis and is now recognized as a regulator of many diseases. Although germ-free mouse models are the standard for microbiome studies, mice with antibiotic-induced sterile intestines are often chosen as a fast and inexpensive alternative. Pathophysiological changes in the gut microbiome have been demonstrated, but there are no reports so far on how such alterations affect the bacterial composition of the uterus. Here we examined changes in uterine microbiota as a result of gut microbiome disruption in an antibiotics-based sterile-uterus mouse model. Sterility was induced in 6-week-old female mice by administration of a combination of antibiotics, and amplicons of a bacteria marker gene (16S rRNA) were sequenced to decipher bacterial community structures in the uterus. At the phylum-level, Proteobacteria, Firmicutes, and Actinobacteria were found to be dominant, while Ralstonia, Escherichia, and Prauserella were the major genera. Quantitative comparisons of the microbial contents of an antibiotic-fed and a control group revealed that the treatment resulted in the reduction of bacterial population density. Although there was no significant difference in bacterial community structures between the two animal groups, β-diversity analysis showed a converged profile of uterus microbiotain the germ-free model. These findings suggest that the induction of sterility does not result in changes in the levels of specific taxa but in a reduction of individual variations in the mouse uterus microbiota, accompanied by a decrease in overall bacterial population density.

키워드

과제정보

This research was supported by the National University Promotion Program at Jeonbuk National University in 2021.

참고문헌

  1. Bai S, Huang B, Fu S, Zhu M, Hu L, Zhu L, Chen M, Zhang Z, Tan J, Zhang J, Chen H (2021) Changes in the distribution of intrauterine microbiota may attribute to immune imbalance in the CBA/J×DBA/2 abortion-prone mice model. Front Immunol 12:641281.
  2. Baker JM, Chase DM, Herbst-Kralovetz MM (2018) Uterine microbiota: Residents, tourists, or invaders? Front Immunol 9:208.
  3. Benner M, Ferwerda G, Joosten I, van der Molen RG (2018) How uterine microbiota might be responsible for a receptive, fertile endometrium. Hum Reprod Update 24:393-415. https://doi.org/10.1093/humupd/dmy012
  4. Franasiak JM, Alecsandru D, Forman EJ, Gemmell LC, Goldberg JM, Llarena N, Margolis C, Laven J, Schoenmakers S, Seli E (2021) A review of the pathophysiology of recurrent implantation failure. Fertil Steril 116:1436-1448. https://doi.org/10.1016/j.fertnstert.2021.09.014
  5. Franasiak JM, Werner MD, Juneau CR, Tao X, Landis J, Zhan Y, Treff NR, Scott RT (2016) Endometrial microbiome at the time of embryo transfer: Next-generation sequencing of the 16S ribosomal subunit. J Assist Reprod Genet 33:129-136. https://doi.org/10.1007/s10815-015-0614-z
  6. Gobbo MM, Bomfim MB, Alves WY, Oliveira KC, Corsetti PP, de Almeida LA (2022) Antibiotic-induced gut dysbiosis and autoimmune disease: A systematic review of preclinical studies. Autoimmun Rev 21:103140.
  7. Hasan RA, Koh AY, Zia A (2020) The gut microbiome and thromboembolism. Thromb Res 189:77-87. https://doi.org/10.1016/j.thromres.2020.03.003
  8. Herlemann DPR, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571-1579. https://doi.org/10.1038/ismej.2011.41
  9. Kennedy EA, King KY, Baldridge MT (2018) Mouse microbiota models: Comparing germ-free mice and antibiotics treatment as tools for modifying gut bacteria. Front Physiol 9:1534.
  10. Knight R, Callewaert C, Marotz C, Hyde ER, Debelius JW, McDonald D, Sogin ML (2017) The microbiome and human biology. Annu Rev Genomics Hum Genet 18:65-86. https://doi.org/10.1146/annurev-genom-083115-022438
  11. Lahiri S, Kim H, Garcia-Perez I, Reza MM, Martin KA, Kundu P, Cox LM, Selkrig J, Posma JM, Zhang H, Padmanabhan P, Moret C, Gulyas B, Blaser MJ, Auwerx J, Holmes E, Nicholson J, Wahli W, Pettersson S (2019) The gut microbiota influences skeletal muscle mass and function in mice. Sci Transl Med 11:eaan5662.
  12. Li J, Pu F, Peng C, Wang Y, Zhang Y, Wu S, Wang S, Shen X, Li Y, Cheng R, He F (2022) Antibiotic cocktail-induced gut microbiota depletion in different stages could cause host cognitive impairment and emotional disorders in adulthood in different manners. Neurobiol Dis 170:105757.
  13. Lin CS, Chang CJ, Lu CC, Martel J, Ojcius DM, Ko YF, Young JD, Lai HC (2014) Impact of the gut microbiota, prebiotics, and probiotics on human health and disease. Biomed J 37:259-268. https://doi.org/10.4103/2319-4170.138314
  14. Livanos AE, Greiner TU, Vangay P, Pathmasiri W, Stewart D, McRitchie S, Li H, Chung J, Sohn J, Kim S, Gao Z, Barber C, Kim J, Ng S, Rogers AB, Sumner S, Zhang XS, Cadwell K, Knights D, Alekseyenko A, Backhed F, Blaser MJ (2016) Antibiotic-mediated gut microbiome perturbation accelerates development of type 1 diabetes in mice. Nat Microbiol 1:16140.
  15. Mitchell CM, Haick A, Nkwopara E, Garcia R, Rendi M, Agnew K, Fredricks DN, Eschenbach D (2015) Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women. Am J Obstet Gynecol 212:611.E1-611.E9.
  16. Palm NW, de Zoete MR, Flavell RA (2015) Immune-microbiota interactions in health and disease. Clin Immunol 159:122-127. https://doi.org/10.1016/j.clim.2015.05.014
  17. Perez-Munoz ME, Arrieta MC, Ramer-Tait AE, Walter J (2017) A critical assessment of the "sterile womb" and "in utero colonization" hypotheses: Implications for research on the pioneer infant microbiome. Microbiome 5:48.
  18. Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA, Bonazzi V, McEwen JE, Wetterstrand KA, Deal C, Baker CC, Francesco VD, Kevin Howcroft T, Karp RW, Dwayne Lunsford R, Wellington CR, Belachew T, Wright M, Giblin C, David H, Mills M, Salomon R, Mullins C, Akolkar B, Begg L, Davis C, Grandison L, Humble1 M, Khalsa J, Roger Little A, Peavy H, Pontzer C, Portnoy M, Sayre MH, Starke-Reed P, Zakhari S, Read J, Watson B, Guyer M (2009) The NIH human microbiome project. Genome Res 19:2317-2323. https://doi.org/10.1101/gr.096651.109
  19. Shojaee AliAbadi F, Lees P (2000) Antibiotic treatment for animals: Effect on bacterial population and dosage regimen optimisation. Int J Antimicrob Agents 14:307-313. https://doi.org/10.1016/S0924-8579(00)00142-4
  20. Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, Zur M, Regev-Lehavi D, Brik RBZ, Federici S, Horn M, Cohen Y, Moor AE, Zeevi D, Korem T, Kotler E, Harmelin A, Itzkovitz S, Maharshak N, Shibolet O, Pevsner-Fischer M, Shapiro H, Sharon I, Halpern Z, Segal E, Elinav E (2018) Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174:1406-1423.E16. https://doi.org/10.1016/j.cell.2018.08.047
  21. Tao X, Franasiak JM, Zhan Y, Scott RT 3rd, Rajchel J, Bedard J, Newby R Jr, Scott RT, Treff NR, Chu T (2017) Characterizing the endometrial microbiome by analyzing the ultra-low bacteria from embryo transfer catheter tips in IVF cycles: Next generation sequencing (NGS) analysis of the 16S ribosomal gene. Hum Microbiome J 3:15-21. https://doi.org/10.1016/j.humic.2017.01.004
  22. Theriot CM, Koenigsknecht MJ, Carlson PE Jr, Hatton GE, Nelson AM, Li B, Huffnagle GB, Li JZ, Young VB (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5:3114.
  23. Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Delanghe J, Van Simaey L, De Ganck C, Temmerman M, Vaneechoutte M (2004) Cloning of 16S rRNA genes amplified from normal and disturbed vaginal microflora suggests a strong association between Atopobium vaginae, Gardnerella vaginalis and bacterial vaginosis. BMC Microbiol 4:16.
  24. Verstraelen H, Vilchez-Vargas R, Desimpel F, Jauregui R, Vankeirsbilck N, Weyers S, Verhelst R, De Sutter P, Pieper DH, Van De Wiele T (2016) Characterisation of the human uterine microbiome in non-pregnant women through deep sequencing of the V1-2 region of the 16S rRNA gene. PeerJ 4:e1602.
  25. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613.