Eukaryome: Emerging Field with Profound Translational Potential

  • Nancy GuillenEmail author
Conference paper


The human intestinal eukaryome comprises a diverse set of eukaryotic organisms living in the intestinal lumen. These are in permanent or transient interaction with commensal organisms such as bacteria. This interaction has a direct impact on human well-being. The eukaryome remains one of the least understood components of the gut microbiota despite its permanent association with the host during the natural selection of species. The emerging work hypothesis is that eukaryome and bacteria in synergy influence the complex mechanism underlying the microbial crosstalk with the human gut during health or disease. New microbiota studies should therefore include the characterization of the components and function of the eukaryome to discover its role in homeostasis and intestinal diseases.


Eukaryome Microbiome Human populations Immune response Tissue models 



NG work was supported by European ERA-NET Infect-ERA program AMOEBAC (French National Agency for Research grant ANR-14-IFEC-0001-02).


  1. Alfellani, M. A., Jacob, A. S., Perea, N. O., Krecek, R. C., Taner-Mulla, D., Verweij, J. J., et al. (2013). Diversity and distribution of Blastocystis sp. subtypes in non-human primates. Parasitology, 140(8), 966–971.PubMedGoogle Scholar
  2. Alivisatos, A. P., Blaser, M. J., Brodie, E. L., Chun, M., Dangl, J. L., Donohue, T. J., et al. (2015). MICROBIOME. A unified initiative to harness Earth’s microbiomes. Science, 350(6260), 507–508.PubMedGoogle Scholar
  3. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., et al. (2011). Induction of colonic regulatory T cells by indigenous Clostridium species. Science, 331(6015), 337–341.PubMedGoogle Scholar
  4. Audebert, C., Even, G., Cian, A., Loywick, A., Merlin, S., Viscogliosi, E., et al. (2016). Colonization with the enteric protozoa Blastocystis is associated with increased diversity of human gut bacterial microbiota. Scientific Reports, 6, 25255.PubMedPubMedCentralGoogle Scholar
  5. Barratt, J. L., Harkness, J., Marriott, D., Ellis, J. T., & Stark, D. (2011). A review of Dientamoeba fragilis carriage in humans: Several reasons why this organism should be considered in the diagnosis of gastrointestinal illness. Gut Microbes, 2(1), 3–12.PubMedGoogle Scholar
  6. Bart, A., Wentink-Bonnema, E. M., Gilis, H., Verhaar, N., Wassenaar, C. J., van Vugt, M., et al. (2013). Diagnosis and subtype analysis of Blastocystis sp. in 442 patients in a hospital setting in the Netherlands. BMC Infectious Diseases, 13, 389.PubMedPubMedCentralGoogle Scholar
  7. Burgess, S. L., Buonomo, E., Carey, M., Cowardin, C., Naylor, C., Noor, Z., et al. (2014). Bone marrow dendritic cells from mice with an altered microbiota provide interleukin 17A-dependent protection against Entamoeba histolytica colitis. MBio, 5(6), e01817.Google Scholar
  8. Burgess, S. L., Oka, A., Liu, B., Bolick, D. T., Oakland, D. N., Guerrant, R. L., et al. (2019). Intestinal parasitic infection alters bone marrow derived dendritic cell inflammatory cytokine production in response to bacterial endotoxin in a diet-dependent manner. PLoS Neglected Tropical Diseases, 13(7), e0007515.PubMedPubMedCentralGoogle Scholar
  9. Burrows, K., Ngai, L., Wong, F., Won, D., & Mortha, A. (2019). ILC2 activation by protozoan commensal microbes. International Journal of Molecular Science, 20(19).Google Scholar
  10. Byers, J., & Eichinger, D. (2008). Acetylation of the Entamoeba histone H4 N-terminal domain is influenced by short-chain fatty acids that enter trophozoites in a pH-dependent manner. International Journal for Parasitology, 38(1), 57–64.PubMedGoogle Scholar
  11. Byers, J., Faigle, W., & Eichinger, D. (2005). Colonic short-chain fatty acids inhibit encystation of Entamoeba invadens. Cellular Microbiology, 7(2), 269–279.PubMedGoogle Scholar
  12. Cardenas, D., Bhalchandra, S., Lamisere, H., Chen, Y., Zeng, X. L., Ramani, S., et al. (2020). Two- and three-dimensional bioengineered human intestinal tissue models for Cryptosporidium. Methods in Molecular Biology, 2052, 373–402.PubMedGoogle Scholar
  13. Chabe, M., Lokmer, A., & Segurel, L. (2017). Gut protozoa: Friends or foes of the human gut microbiota? Trends in Parasitology, 33(12), 925–934.PubMedGoogle Scholar
  14. 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
  15. Cobo, E. R., Kissoon-Singh, V., Moreau, F., Holani, R., & Chadee, K. (2017). MUC2 mucin and butyrate contribute to the synthesis of the antimicrobial peptide cathelicidin in response to Entamoeba histolytica- and dextran sodium sulfate-induced colitis. Infection and Immunity, 85(3).Google Scholar
  16. Cooper, P., Walker, A. W., Reyes, J., Chico, M., Salter, S. J., Vaca, M., et al. (2013). Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE, 8(10), e76573.PubMedPubMedCentralGoogle Scholar
  17. Cornick, S., Moreau, F., Gaisano, H. Y., & Chadee, K. (2017). Entamoeba histolytica-induced mucin exocytosis is mediated by VAMP8 and is critical in mucosal innate host defense. MBio, 8(5).Google Scholar
  18. Costello, C. M., Sorna, R. M., Goh, Y. L., Cengic, I., Jain, N. K., & March, J. C. (2014). 3-D intestinal scaffolds for evaluating the therapeutic potential of probiotics. Molecular Pharmaceutics, 11(7), 2030–2039.PubMedPubMedCentralGoogle Scholar
  19. DeCicco RePass, M. A., Chen, Y., Lin, Y., Zhou, W., Kaplan, D. L., & Ward, H. D. (2017). Novel bioengineered three-dimensional human intestinal model for long-term infection of Cryptosporidium parvum. Infection and Immunity, 85(3).Google Scholar
  20. Desai, M. S., Seekatz, A. M., Koropatkin, N. M., Kamada, N., Hickey, C. A., Wolter, M., et al. (2016). A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell, 167(5), 1339–1353.e1321.PubMedPubMedCentralGoogle Scholar
  21. Dikongue, E., & Segurel, L. (2017). Latitude as a co-driver of human gut microbial diversity? Bioessays, 39(3).Google Scholar
  22. Doll, J. P., & Franker, C. K. (1963). Experimental histomoniasis in gnotobiotic turkeys. I. Infection and histopathology of the bacteria-free host. Journal of Parasitology, 49, 411–414.PubMedGoogle Scholar
  23. Du, Q., Schilde, C., Birgersson, E., Chen, Z. H., McElroy, S., & Schaap, P. (2014). The cyclic AMP phosphodiesterase RegA critically regulates encystation in social and pathogenic amoebas. Cellular Signalling, 26(2), 453–459.PubMedPubMedCentralGoogle Scholar
  24. Dutton, J. S., Hinman, S. S., Kim, R., Wang, Y., & Allbritton, N. L. (2019). Primary cell-derived intestinal models: Recapitulating physiology. Trends in Biotechnology, 37(7), 744–760.PubMedGoogle Scholar
  25. El Safadi, D., Cian, A., Nourrisson, C., Pereira, B., Morelle, C., Bastien, P., et al. (2016). Prevalence, risk factors for infection and subtype distribution of the intestinal parasite Blastocystis sp. from a large-scale multi-center study in France. BMC Infectious Diseases, 16(1), 451.PubMedPubMedCentralGoogle Scholar
  26. Embley, T. M., & Martin, W. (2006). Eukaryotic evolution, changes and challenges. Nature, 440(7084), 623–630.PubMedGoogle Scholar
  27. 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.PubMedGoogle Scholar
  28. Frisbee, A. L., Saleh, M. M., Young, M. K., Leslie, J. L., Simpson, M. E., Abhyankar, M. M., et al. (2019). IL-33 drives group 2 innate lymphoid cell-mediated protection during Clostridium difficile infection. Nature Communications, 10(1), 2712.PubMedPubMedCentralGoogle Scholar
  29. Galvan-Moroyoqui, J. M., Del Carmen Dominguez-Robles, M., Franco, E., & Meza, I. (2008). The interplay between Entamoeba and enteropathogenic bacteria modulates epithelial cell damage. PLoS Neglected Tropical Diseases, 2(7), e266.PubMedPubMedCentralGoogle Scholar
  30. Gerbe, F., Sidot, E., Smyth, D. J., Ohmoto, M., Matsumoto, I., Dardalhon, V., et al. (2016). Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature, 529(7585), 226–230.PubMedGoogle Scholar
  31. Gilchrist, C. A., Petri, S. E., Schneider, B. N., Reichman, D. J., Jiang, N., Begum, S., et al. (2016). Role of the gut microbiota of children in Diarrhea due to the protozoan parasite Entamoeba histolytica. Journal of Infectious Diseases, 213(10), 1579–1585.PubMedGoogle Scholar
  32. Glover, M., Colombo, S. A. P., Thornton, D. J., & Grencis, R. K. (2019). Trickle infection and immunity to Trichuris muris. PLoS Pathogens, 15(11), e1007926.PubMedPubMedCentralGoogle Scholar
  33. Goto, Y. (2019). Epithelial cells as a transmitter of signals from commensal bacteria and host immune cells. Frontiers in Immunology, 10, 2057.PubMedPubMedCentralGoogle Scholar
  34. Gouba, N., & Drancourt, M. (2015). Digestive tract mycobiota: A source of infection. Médecine et Maladies Infectieuses, 45(1–2), 9–16.PubMedGoogle Scholar
  35. Hamad, I., Raoult, D., & Bittar, F. (2016). Repertory of eukaryotes (eukaryome) in the human gastrointestinal tract: Taxonomy and detection methods. Parasite Immunology, 38(1), 12–36.PubMedGoogle Scholar
  36. Heo, I., Dutta, D., Schaefer, D. A., Iakobachvili, N., Artegiani, B., Sachs, N., et al. (2018). Modelling Cryptosporidium infection in human small intestinal and lung organoids. Nature Microbiology, 3(7), 814–823.PubMedPubMedCentralGoogle Scholar
  37. Hess, M., Liebhart, D., Bilic, I., & Ganas, P. (2015). Histomonas meleagridis—New insights into an old pathogen. Veterinary Parasitology, 208(1–2), 67–76.PubMedGoogle Scholar
  38. Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268–1273.PubMedPubMedCentralGoogle Scholar
  39. Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J., & Jacobson, J. (2008). Helminth infections: The great neglected tropical diseases. The Journal of Clinical Investigation, 118(4), 1311–1321.PubMedPubMedCentralGoogle Scholar
  40. 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.PubMedPubMedCentralGoogle Scholar
  41. 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.PubMedPubMedCentralGoogle Scholar
  42. Iebba, V., Santangelo, F., Totino, V., Pantanella, F., Monsia, A., Di Cristanziano, V., et al. (2016). Gut microbiota related to Giardia duodenalis, Entamoeba spp. and Blastocystis hominis infections in humans from Cote d’Ivoire. The Journal of Infection in Developing Countries, 10(9), 1035–1041.PubMedGoogle Scholar
  43. Ivanov, K., II, Atarashi, N., Manel, E. L., Brodie, T., Shima, U., Karaoz, D., et al. (2009). Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell, 139(3), 485–498.PubMedPubMedCentralGoogle Scholar
  44. Iyer, L. R., Verma, A. K., Paul, J., & Bhattacharya, A. (2019). Phagocytosis of gut bacteria by Entamoeba histolytica. Frontiers in Cellular Infection Microbiology, 9, 34.PubMedGoogle Scholar
  45. Jalili-Firoozinezhad, S., Gazzaniga, F. S., Calamari, E. L., Camacho, D. M., Fadel, C. W., Bein, A., et al. (2019). A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nature Biomedical Engineering, 3(7), 520–531.PubMedPubMedCentralGoogle Scholar
  46. Johansson, M. E., Ambort, D., Pelaseyed, T., Schutte, A., Gustafsson, J. K., Ermund, A., et al. (2011). Composition and functional role of the mucus layers in the intestine. Cellular and Molecular Life Sciences, 68(22), 3635–3641.PubMedGoogle Scholar
  47. Kawabe, Y., Schilde, C., Du, Q., & Schaap, P. (2015). A conserved signalling pathway for amoebozoan encystation that was co-opted for multicellular development. Scientific Reports, 5, 9644.PubMedPubMedCentralGoogle Scholar
  48. Kim, H. J., Huh, D., Hamilton, G., & Ingber, D. E. (2012). Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab on a Chip, 12(12), 2165–2174.PubMedGoogle Scholar
  49. Kim, H. J., Li, H., Collins, J. J., & Ingber, D. E. (2016). Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. National Academy of Sciences of the United States of America, 113(1), E7–15.Google Scholar
  50. Lee, S. C., Tang, M. S., Lim, Y. A., Choy, S. H., Kurtz, Z. D., Cox, L. M., et al. (2014). Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Neglected Tropical Diseases, 8(5), e2880.PubMedPubMedCentralGoogle Scholar
  51. Leon-Coria, A., Kumar, M., Moreau, F., & Chadee, K. (2018). Defining cooperative roles for colonic microbiota and Muc2 mucin in mediating innate host defense against Entamoeba histolytica. PLoS Pathogens, 14(11), e1007466.PubMedPubMedCentralGoogle Scholar
  52. Liu, S., Roellig, D. M., Guo, Y., Li, N., Frace, M. A., Tang, K., et al. (2016). Evolution of mitosome metabolism and invasion-related proteins in Cryptosporidium. BMC Genomics, 17(1), 1006.PubMedPubMedCentralGoogle Scholar
  53. Lokmer, A., Cian, A., Froment, A., Gantois, N., Viscogliosi, E., Chabe, M., et al. (2019). Use of shotgun metagenomics for the identification of protozoa in the gut microbiota of healthy individuals from worldwide populations with various industrialization levels. PLoS ONE, 14(2), e0211139.PubMedPubMedCentralGoogle Scholar
  54. Mahapatro, M., Foersch, S., Hefele, M., He, G. W., Giner-Ventura, E., McHedlidze, T., et al. (2016). Programming of intestinal epithelial differentiation by IL-33 derived from pericryptal fibroblasts in response to systemic infection. Cell Reports, 15(8), 1743–1756.PubMedGoogle Scholar
  55. Maizels, R. M., Smits, H. H., & McSorley, H. J. (2018). Modulation of host immunity by Helminths: The expanding repertoire of parasite effector molecules. Immunity, 49(5), 801–818.PubMedPubMedCentralGoogle Scholar
  56. Manna, D., Lentz, C. S., Ehrenkaufer, G. M., Suresh, S., Bhat, A., & Singh, U. (2018).An NAD(+)-dependent novel transcription factor controls stage conversion in Entamoeba. Elife, 7.Google Scholar
  57. Maynard, C. L., Elson, C. O., Hatton, R. D., & Weaver, C. T. (2012). Reciprocal interactions of the intestinal microbiota and immune system. Nature, 489(7415), 231–241.PubMedPubMedCentralGoogle Scholar
  58. McDole, J. R., Wheeler, L. W., McDonald, K. G., Wang, B., Konjufca, V., Knoop, K. A., et al. (2012). Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature, 483(7389), 345–349.PubMedPubMedCentralGoogle Scholar
  59. Mi-ichi, F., Miyamoto, T., Takao, S., Jeelani, G., Hashimoto, T., Hara, H., et al. (2015a). Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis. National Academy of Sciences of the United States of America, 112(22), E2884–2890.Google Scholar
  60. Mi-ichi, F., Nozawa, A., Yoshida, H., Tozawa, Y., & Nozaki, T. (2015b). Evidence that the Entamoeba histolytica mitochondrial carrier family links mitosomal and cytosolic pathways through exchange of 3′-phosphoadenosine 5′-phosphosulfate and ATP. Eukaryotic Cell, 14(11), 1144–1150.PubMedPubMedCentralGoogle Scholar
  61. Mi-ichi, F., Miyamoto, T., & Yoshida, H. (2017). Uniqueness of Entamoeba sulfur metabolism: Sulfolipid metabolism that plays pleiotropic roles in the parasitic life cycle. Molecular Microbiology, 106(3), 479–491.PubMedGoogle Scholar
  62. Miller, A. M. (2011). Role of IL-33 in inflammation and disease. Journal of Inflammation (London), 8(1), 22.Google Scholar
  63. Mmbaga, B. T., & Houpt, E. R. (2017). Cryptosporidium and Giardia infections in children: A review. Pediatric Clinics of North America, 64(4), 837–850.PubMedGoogle Scholar
  64. Morton, E. R., Lynch, J., Froment, A., Lafosse, S., Heyer, E., Przeworski, M., et al. (2015). Variation in rural African gut microbiota is strongly correlated with colonization by entamoeba and subsistence. PLoS Genetics, 11(11), e1005658.PubMedPubMedCentralGoogle Scholar
  65. Nieves-Ramirez, M. E., Partida-Rodriguez, O., Laforest-Lapointe, I., Reynolds, L. A., Brown, E. M., Valdez-Salazar, A., et al. (2018). Asymptomatic intestinal colonization with protist Blastocystis is strongly associated with distinct microbiome ecological patterns. MSystems, 3(3).Google Scholar
  66. Ohshima, K., Kanto, K., Hatakeyama, K., Ide, T., Wakabayashi-Nakao, K., Watanabe, Y., et al. (2014). Exosome-mediated extracellular release of polyadenylate-binding protein 1 in human metastatic duodenal cancer cells. Proteomics, 14(20), 2297–2306.PubMedGoogle Scholar
  67. Parfrey, L. W., Walters, W. A., & Knight, R. (2011). Microbial eukaryotes in the human microbiome: Ecology, evolution, and future directions. Frontiers in Microbiology, 2, 153.PubMedPubMedCentralGoogle Scholar
  68. 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. Frontiers in Microbiology, 5, 298.PubMedPubMedCentralGoogle Scholar
  69. Pelaseyed, T., Bergstrom, J. H., Gustafsson, J. K., Ermund, A., Birchenough, G. M., Schutte, A., et al. (2014). The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunological Reviews, 260(1), 8–20.PubMedPubMedCentralGoogle Scholar
  70. Peng, L., Li, Z. R., Green, R. S., Holzman, I. R., & Lin, J. (2009). Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. Journal of Nutrition, 139(9), 1619–1625.PubMedGoogle Scholar
  71. Proctor, L. M., Creasy, H. H., Fettweis, J. M., Lloyd-Price, J., Mahurkar, A., Zhou, W., et al. (2019). The integrative human microbiome project. Nature, 569(7758), 641–648.Google Scholar
  72. Pullan, R. L., Smith, J. L., Jasrasaria, R., & Brooker, S. J. (2014). Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites and Vectors, 7, 37.PubMedGoogle Scholar
  73. Ramirez, J. D., Sanchez, L. V., Bautista, D. C., Corredor, A. F., Florez, A. C., & Stensvold, C. R. (2014). Blastocystis subtypes detected in humans and animals from Colombia. Infection, Genetics and Evolution, 22, 223–228.PubMedGoogle Scholar
  74. Reinoso Webb, C., Koboziev, I., Furr, K. L., & Grisham, M. B. (2016). Protective and pro-inflammatory roles of intestinal bacteria. Pathophysiology, 23(2), 67–80.PubMedGoogle Scholar
  75. Robertson, L. J., Clark, C. G., Debenham, J. J., Dubey, J. P., Kvac, M., Li, J., et al. (2019). Are molecular tools clarifying or confusing our understanding of the public health threat from zoonotic enteric protozoa in wildlife? The International Journal for Parasitology: Parasites and Wildlife, 9, 323–341.PubMedGoogle Scholar
  76. Rojas, A. A., Castro, S. C., Matondo, M., Gianetto, Q. G., Varet, H., Sismeiro, O., Legendre, R., Fernandes, J., Hardy, D., Coppée, J. Y., Olivo-Marin, J. C., & Guillen, N. (2020). Insights into amebiasis using a human-intestinal model. Cellular Microbiology, Mar 16:e13203.
  77. 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.PubMedPubMedCentralGoogle Scholar
  78. Shaulov, Y., Shimokawa, C., Trebicz-Geffen, M., Nagaraja, S., Methling, K., Lalk, M., et al. (2018). Escherichia coli mediated resistance of Entamoeba histolytica to oxidative stress is triggered by oxaloacetate. PLoS Pathogens, 14(10), e1007295.PubMedPubMedCentralGoogle Scholar
  79. Shiflett, A. M., & Johnson, P. J. (2010). Mitochondrion-related organelles in eukaryotic protists. Annual Review of Microbiology, 64, 409–429.PubMedPubMedCentralGoogle Scholar
  80. Shin, W., & Kim, H. J. (2018). Pathomimetic modeling of human intestinal diseases and underlying host-gut microbiome interactions in a gut-on-a-chip. Methods in Cell Biology, 146, 135–148.PubMedGoogle Scholar
  81. Steele, S. P., Melchor, S. J., & Petri, W. A., Jr. (2016). Tuft cells: New players in colitis. Trends in Molecular Medicine, 22(11), 921–924.PubMedPubMedCentralGoogle Scholar
  82. Thursby, E., & Juge, N. (2017). Introduction to the human gut microbiota. Biochemical Journal, 474(11), 1823–1836.PubMedPubMedCentralGoogle Scholar
  83. Troeger, C., Forouzanfar, M., Rao, P. C., Khalil, I., Brown, A., & Reiner, R. C. Jr. (2017). Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: A systematic analysis for the Global Burden of Disease Study 2015. Lancet Infectious Diseases, 17(9), 909–948.Google Scholar
  84. Tovaglieri, A., Sontheimer-Phelps, A., Geirnaert, A., Prantil-Baun, R., Camacho, D. M., Chou, D. B., et al. (2019). Species-specific enhancement of enterohemorrhagic E. coli pathogenesis mediated by microbiome metabolites. Microbiome, 7(1), 43.PubMedPubMedCentralGoogle Scholar
  85. Varet, H., Shaulov, Y., Sismeiro, O., Trebicz-Geffen, M., Legendre, R., Coppee, J. Y., et al. (2018). Enteric bacteria boost defences against oxidative stress in Entamoeba histolytica. Scientific Reports, 8(1), 9042.PubMedPubMedCentralGoogle Scholar
  86. Verma, A. K., Verma, R., Ahuja, V., & Paul, J. (2012). Real-time analysis of gut flora in Entamoeba histolytica infected patients of Northern India. BMC Microbiology, 12, 183.PubMedPubMedCentralGoogle Scholar
  87. von Moltke, J., Ji, M., Liang, H. E., & Locksley, R. M. (2016). Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature, 529(7585), 221–5.Google Scholar
  88. Wang, Y., Ahmad, A. A., Sims, C. E., Magness, S. T., & Allbritton, N. L. (2014). In vitro generation of colonic epithelium from primary cells guided by microstructures. Lab on a Chip, 14(9), 1622–1631.PubMedPubMedCentralGoogle Scholar
  89. Wang, Y., Kim, R., Sims, C. E., & Allbritton, N. L. (2019). Building a thick mucus hydrogel layer to improve the physiological relevance of in vitro primary colonic Epithelial models. Cellular and Molecular Gastroenterology and Hepatology, 8(4), 653–655.e655.PubMedPubMedCentralGoogle Scholar
  90. Watanabe, K., Gilchrist, C. A., Uddin, M. J., Burgess, S. L., Abhyankar, M. M., Moonah, S. N., et al. (2017). Microbiome-mediated neutrophil recruitment via CXCR2 and protection from amebic colitis. PLoS Pathogens, 13(8), e1006513.PubMedPubMedCentralGoogle Scholar
  91. Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., et al. (2012). Human gut microbiome viewed across age and geography. Nature, 486(7402), 222–227.PubMedPubMedCentralGoogle Scholar
  92. Zindl, C. L., Lai, J. F., Lee, Y. K., Maynard, C. L., Harbour, S. N., Ouyang, W., et al. (2013). IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. National Academy of Sciences of the United States of America, 110(31), 12768–12773.Google Scholar

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Authors and Affiliations

  1. 1.Institut PasteurCentre National de la Recherche Scientifique-ERL9195ParisFrance

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