DOI QR코드

DOI QR Code

Home-Field Advantage: Why Host-Specificity is Important for Therapeutic Microbial Engraftment

  • Tyler J. Long (Department of Medicine, University of Massachusetts T.H. Chan Medical School)
  • Received : 2022.12.07
  • Accepted : 2023.01.18
  • Published : 2023.03.28

Abstract

Among certain animals, gut microbiomes demonstrate species-specific patterns of beta diversity. This host-specificity is a potent driver of exogenous microbial exclusion. To overcome persistent translational limitations, translational microbiome research and therapeutic development must account for host-specific patterns of microbial engraftment. This commentary seeks to highlight the important implications of host-specificity for microbial ecology, Fecal Microbiota Transplantation (FMT), next-generation probiotics, and translational microbiota research.

Keywords

Acknowledgement

The author would like to thank the members of the Chang lab at the University of Chicago for discussions and critical reading, particularly Na Fei, PhD and Eugene Chang, PhD. This work was funded by grants from the National Institutes of Health (RC2DK122394).

References

  1. Ley RE, Hamady M, Catherine L, Turnbaugh PJ, Ramey RR, Stephen Bircher J, et al. 2008. Evolution of mammals and their gut microbes. Science 320: 1647-1651. https://doi.org/10.1126/science.1155725
  2. Neff EP. 2020. Of microbiome and metabolome in the bobtail squid. Lab. Anim. 49: 316-316. https://doi.org/10.1038/s41684-020-00670-2
  3. Mallott EK, Amato KR. 2021. Host specificity of the gut microbiome. Nat. Rev. Microbiol. 19: 639-653. https://doi.org/10.1038/s41579-021-00562-3
  4. Brucker RM, Bordenstein SR. 2013. The hologenomic basis of speciation: Gut bacteria cause hybrid lethality in the genus nasonia. Science 341: 667-669. https://doi.org/10.1126/science.1240659
  5. Brooks AW, Kohl KD, Brucker RM, Opstal EJ van, Bordenstein SR. 2016. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 14: e2000225.
  6. Davenport ER, Sanders JG, Song SJ, Amato KR, Clark AG, Knight R. 2017. The human microbiome in evolution. BMC Biol. 15: 127.
  7. Beasley DE, Koltz AM, Lambert JE, Fierer N, Dunn RR. 2015. The evolution of stomach acidity and its relevance to the human microbiome. PLoS One 10: e0134116.
  8. Lawley TD, Walker AW. 2013. Intestinal colonization resistance. Immunology 138: 1-11. https://doi.org/10.1111/j.1365-2567.2012.03616.x
  9. Bibbo S, Lopetuso LR, Ianiro G, Di Rienzo T, Gasbarrini A, Cammarota G. 2014. Role of microbiota and innate immunity in recurrent Clostridium difficile infection. J. Immunol. Res. 2014: 462740.
  10. Pan X, Yang Y, Zhang J-R. 2014. Molecular basis of host specificity in human pathogenic bacteria. Emerg. Microbes Infect. 3: e23.
  11. Shepherd ES, DeLoache WC, Pruss KM, Whitaker WR, Sonnenburg JL. 2018. An exclusive metabolic niche enables strain engraftment in the gut microbiota. Nature 557: 434-438. https://doi.org/10.1038/s41586-018-0092-4
  12. Donskey CJ. 2004. The role of the intestinal tract as a reservoir and source for transmission of nosocomial pathogens. Clin. Infect. Dis. 39: 219-226. https://doi.org/10.1086/422002
  13. Park H, Laffin MR, Jovel J, Millan B, Hyun JE, Hotte N, et al. 2019. The success of fecal microbial transplantation in Clostridium difficile infection correlates with bacteriophage relative abundance in the donor: a retrospective cohort study. Gut Microbes 10: 676-687. https://doi.org/10.1080/19490976.2019.1586037
  14. Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M, Bashiardes S, et al. 2018. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174: 1388-1405.e21. https://doi.org/10.1016/j.cell.2018.08.041
  15. Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, et al. 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
  16. Bajinka O, Tan Y, Abdelhalim KA, Ozdemir G, Qiu X. 2020. Extrinsic factors influencing gut microbes, the immediate consequences and restoring eubiosis. AMB Express 10: 130.
  17. Walter J, Maldonado-Gomez MX, Martinez I. 2018. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes. Curr. Opin. Biotechnol. 49: 129-139. https://doi.org/10.1016/j.copbio.2017.08.008
  18. Russell BJ, Brown SD, Siguenza N, Mai I, Saran AR, Lingaraju A, et al. 2022. Intestinal transgene delivery with native E. coli chassis allows persistent physiological changes. Cell 185: 3263-3277.e15. https://doi.org/10.1016/j.cell.2022.06.050
  19. Walter J, Armet AM, Finlay BB, Shanahan F. 2020. Establishing or exaggerating causality for the gut microbiome: Lessons from human microbiota-associated rodents. Cell 180: 221-232. https://doi.org/10.1016/j.cell.2019.12.025
  20. Nguyen TLA, Vieira-Silva S, Liston A, Raes J. 2015. How informative is the mouse for human gut microbiota research? Dis. Model. Mech. 8: 1-16. https://doi.org/10.1242/dmm.017400
  21. Arrieta M-C, Walter J, Finlay BB. 2016. Human microbiota-associated mice: A model with challenges. Cell Host Microbe 19: 575-578. https://doi.org/10.1016/j.chom.2016.04.014