Skip to main content

Tritrichomonas spp. and Their Impact on Gut Immune Homeostasis

  • Conference paper
  • First Online:
Eukaryome Impact on Human Intestine Homeostasis and Mucosal Immunology

Abstract

The intestinal microbiota, the collection of all microorganisms residing in our gastrointestinal tract, provides a plethora of microbial diversity. Bacteria, viruses, fungi, worms and protozoa are the primary microorganisms comprising our microbiota. These microbes include representative species capable of both causing severe harm or symbiotic benefits to their host. In relation, the host immune system has evolved complex detection systems to identify members of each microbial faction and interpret their harmful or peaceful capabilities. As a consequence, our immune system mounts appropriate responses to either eliminate or tolerate members of our microbiota. Protozoa are an underappreciated kingdom within our microbiota and the interactions of these microbes with our immune system remain understudied. Several recent reports have demonstrated that the presence of Tritrichomonas spp. in the intestinal tract of mice and men facilitates novel interactions with our host immune system. Within this chapter, we are summarizing the most recent knowledge on how Tritrichomonads, as a newly emerging group of intestinal protozoan commensals, shape and communicate with our intestinal immune system.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Belkaid, Y., & Hand, T. W. (2014). Role of the microbiota in immunity and inflammation. Cell, 157(1), 121–141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bemark, M., Boysen, P., & Lycke, N. Y. (2012). Induction of gut IgA production through T cell-dependent and T cell-independent pathways. Annals of the New York Academy of Sciences, 1247, 97–116.

    Article  CAS  PubMed  Google Scholar 

  • Benchimol, M., de Almeida, L. G. P., Vasconcelos, A. T., de Andrade Rosa, I., Reis Bogo, M., Kist, L. W., & de Souza, W. (2017). Draft genome sequence of tritrichomonas foetus strain K. Genome Announc, 5(16).

    Google Scholar 

  • Bogunovic, M., Mortha, A., Muller, P. A., & Merad, M. (2012). Mononuclear phagocyte diversity in the intestine. Immunologic Research, 54(1–3), 37–49.

    Article  PubMed  Google Scholar 

  • Boulianne, B., Le, M. X., Ward, L. A., Meng, L., Haddad, D., Li, C., et al. (2013). AID-expressing germinal center B cells cluster normally within lymph node follicles in the absence of FDC-M1+ CD35+ follicular dendritic cells but dissipate prematurely. Journal Immunology, 191(9), 4521–4530.

    Article  CAS  Google Scholar 

  • Burrows, K., Ngai, L., Wong, F., Won, D., & Mortha, A. (2019). ILC2 activation by protozoan commensal microbes. International Journal of Molecular Sciences, 20(19).

    Google Scholar 

  • Cerutti, A. (2008). The regulation of IgA class switching. Nature Reviews Immunology, 8(6), 421–434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan, A. H., & Schroder, K. (2019). Inflammasome signaling and regulation of interleukin-1 family cytokines. Journal of Experimental Medicine.

    Google Scholar 

  • Chudnovskiy, A., Mortha, A., Kana, V., Kennard, A., Ramirez, J. D., Rahman, A., et al. (2016). Host-protozoan interactions protect from mucosal infections through activation of the inflammasome. Cell, 167(2), 444–456, e414.

    Google Scholar 

  • Conrad, M. D., Bradic, M., Warring, S. D., Gorman, A. W., & Carlton, J. M. (2013). Getting Trichy: Tools and approaches to interrogating Trichomonas vaginalis in a post-genome world. Trends in Parasitology, 29(1), 17–25.

    Article  PubMed  Google Scholar 

  • diCenzo, G. C., & Finan, T. M. (2017). The divided bacterial genome: Structure, function, and evolution. Microbiology and Molecular Biology Reviews, 81(3).

    Google Scholar 

  • Dinan, T. G., & Cryan, J. F. (2017). The microbiome-gut-brain axis in health and disease. Gastroenterology Clinics of North America, 46(1), 77–89.

    Article  PubMed  Google Scholar 

  • Embree, J. E. (1998). Dientamoeba fragilis: A harmless commensal or a mild pathogen? Paediatrics & Child Health, 3(2), 81–82.

    Article  Google Scholar 

  • Escalante, N. K., Lemire, P., Cruz Tleugabulova, M., Prescott, D., Mortha, A., Streutker, C. J., et al. (2016). The common mouse protozoa Tritrichomonas muris alters mucosal T cell homeostasis and colitis susceptibility. Journal of Experimental Medicine, 213(13), 2841–2850.

    Article  CAS  Google Scholar 

  • Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D., & Anderton, S. M. (2002). B cells regulate autoimmunity by provision of IL-10. Nature Immunology, 3(10), 944–950.

    Article  CAS  PubMed  Google Scholar 

  • Filyk, H. A., & Osborne, L. C. (2016). The multibiome: The intestinal ecosystem’s influence on immune homeostasis, health, and disease. EBioMedicine, 13, 46–54.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilbert, J. A., Blaser, M. J., Caporaso, J. G., Jansson, J. K., Lynch, S. V., & Knight, R. (2018). Current understanding of the human microbiome. Nature Medicine, 24(4), 392–400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorfu, G., Cirelli, K. M., Melo, M. B., Mayer-Barber, K., Crown, D., Koller, B. H., et al. (2014). Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. MBio, 5(1).

    Google Scholar 

  • Goto, Y., Obata, T., Kunisawa, J., Sato, S., Ivanov, A., II, Lamichhane, N., et al. (2014). Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science, 345(6202), 1254009.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gould, A. L., Zhang, V., Lamberti, L., Jones, E. W., Obadia, B., Korasidis, N., et al. (2018). Microbiome interactions shape host fitness. Proc Natl Acad Sci U S A, 115(51), E11951–E11960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould, S. B., Woehle, C., Kusdian, G., Landan, G., Tachezy, J., Zimorski, V., et al. (2013). Deep sequencing of Trichomonas vaginalis during the early infection of vaginal epithelial cells and amoeboid transition. International Journal for Parasitology, 43(9), 707–719.

    Article  CAS  PubMed  Google Scholar 

  • Gu, N. Y., Kim, J. H., Han, I. H., Im, S. J., Seo, M. Y., Chung, Y. H., et al. (2016). Trichomonas vaginalis induces IL-1beta production in a human prostate epithelial cell line by activating the NLRP3 inflammasome via reactive oxygen species and potassium ion efflux. Prostate, 76(10), 885–896.

    Article  CAS  PubMed  Google Scholar 

  • Hernandez, C. J., Guss, J. D., Luna, M., & Goldring, S. R. (2016). Links between the microbiome and bone. Journal of Bone and Mineral Research, 31(9), 1638–1646.

    Article  PubMed  Google Scholar 

  • Howitt, M. R., Lavoie, S., Michaud, M., Blum, A. M., Tran, S. V., Weinstock, J. V., et al. (2016). Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science, 351(6279), 1329–1333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hrdy, I., Hirt, R. P., Dolezal, P., Bardonova, L., Foster, P. G., Tachezy, J., et al. (2004). Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature, 432(7017), 618–622.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Y., Mao, K., Chen, X., Sun, M. A., Kawabe, T., Li, W., et al. (2018). S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense. Science, 359(6371), 114–119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • International Helminth Genomes, C. (2019). Comparative genomics of the major parasitic worms. Nature Genetics, 51(1), 163–174.

    Article  CAS  Google Scholar 

  • Johnson, P. J., Lahti, C. J., & Bradley, P. J. (1993). Biogenesis of the hydrogenosome in the anaerobic protist Trichomonas vaginalis. Journal of Parasitology, 79(5), 664–670.

    Article  CAS  Google Scholar 

  • Lei, W., Ren, W., Ohmoto, M., Urban, J. F., Jr., Matsumoto, I., Margolskee, R. F., et al. (2018). Activation of intestinal tuft cell-expressed Sucnr1 triggers type 2 immunity in the mouse small intestine. Proceedings of the National Academy of Sciences of the United States of America, 115(21), 5552–5557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, X. V., Leonardi, I., & Iliev, I. D. (2019). Gut mycobiota in immunity and inflammatory disease. Immunity, 50(6), 1365–1379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macpherson, A. J., & Slack, E. (2007). The functional interactions of commensal bacteria with intestinal secretory IgA. Current Opinion in Gastroenterology, 23(6), 673–678.

    Article  CAS  PubMed  Google Scholar 

  • Maritz, J. M., Land, K. M., Carlton, J. M., & Hirt, R. P. (2014). What is the importance of zoonotic trichomonads for human health? Trends in Parasitology, 30(7), 333–341.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maruvada, P., Leone, V., Kaplan, L. M., & Chang, E. B. (2017). The human microbiome and obesity: Moving beyond associations. Cell Host & Microbe, 22(5), 589–599.

    Article  CAS  Google Scholar 

  • Merad, M., Sathe, P., Helft, J., Miller, J., & Mortha, A. (2013). The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annual Review of Immunology, 31, 563–604.

    Article  CAS  PubMed  Google Scholar 

  • Mohanta, T. K., & Bae, H. (2015). The diversity of fungal genome. Biological Procedures Online, 17, 8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mortha, A., & Burrows, K. (2018). Cytokine networks between innate lymphoid cells and myeloid cells. Frontiers in Immunology, 9, 191.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., & Honjo, T. (2000). Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell, 102(5), 553–563.

    Article  CAS  PubMed  Google Scholar 

  • Nadjsombati, M. S., McGinty, J. W., Lyons-Cohen, M. R., Jaffe, J. B., DiPeso, L., Schneider, C., et al. (2018). Detection of succinate by intestinal tuft cells triggers a type 2 innate immune circuit. Immunity, 49(1), 33–41, e37.

    Google Scholar 

  • Okamoto, S., Wakui, M., Kobayashi, H., Sato, N., Ishida, A., Tanabe, M., et al. (1998). Trichomonas foetus meningoencephalitis after allogeneic peripheral blood stem cell transplantation. Bone Marrow Transplantation, 21(1), 89–91.

    Article  CAS  PubMed  Google Scholar 

  • Okamura, H., Tsutsi, H., Komatsu, T., Yutsudo, M., Hakura, A., Tanimoto, T., et al. (1995). Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature, 378(6552), 88–91.

    Article  CAS  PubMed  Google Scholar 

  • Parfrey, L. W., Walters, W. A., Lauber, C. L., Clemente, J. C., Berg-Lyons, D., Teiling, C., et al. (2014). Communities of microbial eukaryotes in the mammalian gut within the context of environmental eukaryotic diversity. Frontier in Microbiology, 5, 298.

    Google Scholar 

  • Pickard, J. M., Maurice, C. F., Kinnebrew, M. A., Abt, M. C., Schenten, D., Golovkina, T. V., et al. (2014). Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature, 514(7524), 638–641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rojas, O. L., Probstel, A. K., Porfilio, E. A., Wang, A. A., Charabati, M., Sun, T., et al. (2019). Recirculating intestinal IgA-producing cells regulate neuroinflammation via IL-10. Cell, 176(3), 610–624, e618.

    Google Scholar 

  • Rooks, M. G., & Garrett, W. S. (2016). Gut microbiota, metabolites and host immunity. Nature Reviews Immunology, 16(6), 341–352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanos, S. L., Bui, V. L., Mortha, A., Oberle, K., Heners, C., Johner, C., et al. (2009). RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nature Immunology, 10(1), 83–91.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, C., Lee, J., Koga, S., Ricardo-Gonzalez, R. R., Nussbaum, J. C., Smith, L. K., et al. (2019). Tissue-resident group 2 innate lymphoid cells differentiate by layered ontogeny and in situ perinatal priming. Immunity, 50(6), 1425–1438, e1425.

    Google Scholar 

  • Schneider, C., O’Leary, C. E., von Moltke, J., Liang, H. E., Ang, Q. Y., Turnbaugh, P. J., et al. (2018). A metabolite-triggered tuft cell-ILC2 circuit drives small intestinal remodeling. Cell, 174(2), 271–284, e214.

    Google Scholar 

  • Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly, Y. M., et al. (2013). The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science, 341(6145), 569–573.

    Article  CAS  PubMed  Google Scholar 

  • Stark, D., Barratt, J., Chan, D., & Ellis, J. T. (2016). Dientamoeba fragilis, the neglected trichomonad of the human bowel. Clinical Microbiology Reviews, 29(3), 553–580.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stavnezer, J., Guikema, J. E., & Schrader, C. E. (2008). Mechanism and regulation of class switch recombination. Annual Review of Immunology, 26, 261–292.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki, J., Kobayashi, S., Osuka, H., Kawahata, D., Oishi, T., Sekiguchi, K., et al. (2016). Characterization of a human isolate of Tritrichomonas foetus (cattle/swine genotype) infected by a zoonotic opportunistic infection. Journal of Veterinary Medical Science, 78(4), 633–640.

    Article  CAS  Google Scholar 

  • Takeuchi, O., & Akira, S. (2010). Pattern recognition receptors and inflammation. Cell, 140(6), 805–820.

    Article  CAS  PubMed  Google Scholar 

  • Tezuka, H., Abe, Y., Asano, J., Sato, T., Liu, J., Iwata, M., et al. (2011). Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity, 34(2), 247–257.

    Article  CAS  PubMed  Google Scholar 

  • Zalonis, C. A., Pillay, A., Secor, W., Humburg, B., & Aber, R. (2011). Rare case of trichomonal peritonitis. Emerging Infectious Diseases, 17(7), 1312–1313.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu, P., Zhu, X., Wu, J., He, L., Lu, T., Wang, Y., et al. (2019). IL-13 secreted by ILC2s promotes the self-renewal of intestinal stem cells through circular RNA circPan3. Nature Immunology, 20(2), 183–194.

    Article  CAS  PubMed  Google Scholar 

  • Zielinski, C. E., Mele, F., Aschenbrenner, D., Jarrossay, D., Ronchi, F., Gattorno, M., et al. (2012). Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature, 484(7395), 514–518.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

E.Y.C. and A.M. would like to thank all members of #theonlylabever for their continued support and discussions. Figure 10.1 was created with BioRender.

Funding

A.M. is supported by CIHR-Project Grant (388337) and NSERC-Discovery Grant (RGPIN-2019-04521). A.M. is the Tier 2 Canadian Research Chair in Mucosal Immunology and supported by the Tier 2 CRC-CIHR program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arthur Mortha .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this paper

Check for updates. Verify currency and authenticity via CrossMark

Cite this paper

Cao, E.Y., Mortha, A. (2020). Tritrichomonas spp. and Their Impact on Gut Immune Homeostasis. In: Guillen, N. (eds) Eukaryome Impact on Human Intestine Homeostasis and Mucosal Immunology. Springer, Cham. https://doi.org/10.1007/978-3-030-44826-4_10

Download citation

Publish with us

Policies and ethics