Abstract
The human intestinal microbiota is composed of a complex combination of microorganisms including bacteria, virus, and eukaryotes. The microbiota plays a critical role in homeostasis through creating a mucosal barrier, providing protective responses to pathogens, and affecting the immune system and metabolism of the host. Molecules secreted by parasites can alter composition of microbiota both by acting directly on the microbial community and indirectly by affecting the host physiology. On the other hand, the microbiota composition can affect the survival, physiology, and virulence of many parasitic protozoa. Explanation of possible interactions between the microbiota, immune response, and protozoa may further clarify the underlying mechanisms of infectivity, clinical variations, and life-cycle of protozoa.
This is a preview of subscription content, log in via an institution to check access.
References
Bär AK, Phukan N, Pinheiro J, Simoes-Barbosa A (2015) The interplay of host microbiota and parasitic protozoans at mucosal interfaces. Implications for the outcomes of infections and diseases. PLOS Neglec Trop Dis. https://doi.org/10.1371/journal.pntd.0004176
Bashey F (2015) Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2014.0301
Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157(1):121–141. https://doi.org/10.1016/j.cell.2014.03.011
Berrilli F, Di Cave D, Cavallero S, D’Amelio S (2012) Interactions between parasites and microbial communities in the human gut. Front Cell Infect Microbiol 2:141. https://doi.org/10.3389/fcimb.2012.00141
Buffie CG, Pamer EG (2013) Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 13(11):790–801. https://doi.org/10.1038/nri3535
Burgess SL, Buonomo E, Carey M, Cowardin C, Naylor C, Noor Z, Wills-Karp M, Petri WA (2014) Bone marrow dendritic cells from mice with an altered microbiota provide interleukin 17A-dependent protection against entamoeba histolytica colitis. PLoS ONE. https://doi.org/10.1371/journal.pone.0158979
Burgess SL, Gilchrist CA, Lynn TC, Petri WA (2017) Parasitic protozoa and interactions with the host intestinal microbiota. Infect Immun 85(8):e00101-e117. https://doi.org/10.1128/IAI.00101-17
Chappell CL, Darkoh C, Shimmin L, Farhana N, Kim DK, Okhuysen PC, Hixson J (2016) Fecal indole as a biomarker of susceptibility to Cryptosporidium infection. Infect Immun 84(8):2299–2306. https://doi.org/10.1128/IAI.00336-16
Fujimura KE, Lynch SV (2015) Microbiota in allergy and asthma and the emerging relationship with the gut microbiome. Cell Host Microbe 17(5):592–602. https://doi.org/10.1016/j.chom.2015.04.007
Fulbright LE, Ellermann M, Arthur JC (2017) The microbiome and the hallmarks of cancer. PLOS Pathog. https://doi.org/10.1371/journal.ppat.1006480
Gilchrist CA, Petri SE, Schneider BN, Reichman DJ, Jiang N, Begum S, Watanabe K, Jansen CS, Elliott KP, Burgess SL, Ma JZ, Alam M, Kabir M, Haque R, Petri WA (2016) Role of the gut microbiota of children in diarrhea due to the protozoan parasite entamoeba histolytica. J Infect Dis 213:1579–1585. https://doi.org/10.1093/infdis/jiv772
Hanevik K, Wensaas KA, Rortveit G, Eide GE, Mørch K, Langeland N (2014) Irritable bowel syndrome and chronic fatigue 6 years after Giardia infection: a controlled prospective cohort study. Clin Infect Dis 59(10):1394–1400. https://doi.org/10.1093/cid/ciu629
Haque R, Huston CD, Hughes M, Houpt E, Petri WA (2003) Amebiasis. N Engl J Med 348(16):1565–1573. https://doi.org/10.1056/NEJMra022710
Hinderfeld AS, Simoes-Barbosa A (2020) Vaginal dysbiotic bacteria act as pathobionts of the protozoal pathogen Trichomonas vaginalis. Microb Pathog 138:103820. https://doi.org/10.1016/j.micpath.2019.103820
Iebba V, Santangelo F, Totino V, Pantanella F, Monsia A, Di Cristanziano V, Di Cave D, Schippa S, Berrilli F, D’Alfonso R (2016) Gut microbiota related to Giardia duodenalis, Entamoeba spp. and Blastocystis hominis infections in humans from Côte D’ivoire. J Infect Dev Countries 10(9):1035–1041. https://doi.org/10.2478/s11686-019-00044-w
Jin UH, Lee SO, Sridharan G, Lee K, Davidson LA, Jayaraman A, Chapkin RS, Alaniz R, Safe S (2014) Microbiome-derived tryptophan metabolites and their aryl hydrocarbon receptor-dependent agonist and antagonist activities. Mol Pharmacol 85(5):777–788. https://doi.org/10.1124/mol.113.091165
Kosek M, Alcantara C, Lima AA, Guerrant RL (2001) Cryptosporidiosis: an update. Lancet Infect Dis 1(4):262–269
Marie C, Petri WA (2014) Regulation of virulence of Entamoeba histolytica. Annu Rev Microbiol 68:493–520. https://doi.org/10.1146/annurev-micro-091313-103550
Mooney JP, Lokken KL, Byndloss MX, George MD, Velazquez EM, Faber F, Butler BP, Walker GT, Ali MM, Potts R, Tiffany C, Ahmer BMM, Luckhart S, Tsolis RM (2015) Inflammation-associated alterations to the intestinal microbiota reduce colonization resistance against non-typhoidal Salmonella during concurrent malaria parasite infection. Sci Rep 5:14603. https://doi.org/10.1038/srep14603
Morton ER, Lynch J, Froment A, Lafosse S, Heyer E, Przeworski M, Blekhman R, Ségurel L (2015) Variation in rural African gut microbiota is strongly correlated with colonization by Entamoeba and subsistence. PLoS Genet. https://doi.org/10.1371/journal.pgen.1005658
Mukherjee D, Chora ÂF, Mota MM (2020) Microbiota, a third player in the host–Plasmodium affair. Trends Parasitol 36(1):11–18. https://doi.org/10.1016/j.pt.2019.11.001
Netea MG, Joosten LAB, Latz E, Mills KHG, Natoli G, Stunnenberg HG, O’Neill LAJ, Xavier RJ (2016) Trained immunity: a program of innate immune memory in health and disease. Science 352(6284):aaf1098. https://doi.org/10.1126/science.aaf1098
O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7(7):688–693. https://doi.org/10.1038/sj.embor.7400731
Pérez PF, Minnaard J, Rouvet M, Knabenhans C, Brassart D, De Antoni GL, Schiffrin EJ (2001) Inhibition of Giardia intestinalis by extracellular factors from lactobacilli: an in vitro study. Appl Environ Microbiol 67(11):5037–5042. https://doi.org/10.1128/AEM.67.11.5037-5042.2001
Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904. https://doi.org/10.1152/physrev.00045.2009
Shanahan F (2002) The host-microbe interface within the gut. Bailliere’s Best Pract Res Clin Gastroenterol 16(6):915–931. https://doi.org/10.1053/bega.2002.0342
Solaymani-Mohammadi S, Singer SM (2010) Giardia duodenalis: the double-edged sword of immune responses in giardiasis. Exp Parasitol 126(3):292–297. https://doi.org/10.1016/j.exppara.2010.06.014
Taniguchi T, Miyauchi E, Nakamura S, Hirai M, Suzue K, Imai T, Nomura T, Handa T, Okada H, Shimokawa C, Onishi R, Olia A, Hirata J, Tomita H, Ohno H, Horii T, Hisaeda H (2015) Plasmodium berghei ANKA causes intestinal malaria associated with dysbiosis. Sci Rep 5:1–13. https://doi.org/10.1038/srep15699
Villarino NF, LeCleir GR, Denny JE, Dearth SP, Harding CL, Sloan SS, Gribble JL, Campagna SR, Wilhelm SW, Schmidt NW (2016) Composition of the gut microbiota modulates the severity of malaria. Proc Natl Acad Sci USA 113(8):2235–2240. https://doi.org/10.1073/pnas.1504887113
Wensaas KA, Langeland N, Hanfvevik K, Mørch K, Eide GE, Rortveit G (2012) Irritable bowel syndrome and chronic fatigue 3 years after acute giardiasis: historic cohort study. Gut 61(2):214–219. https://doi.org/10.1136/gutjnl-2011-300220
World Health Organization (2014) Prevalence and incidence of selected sexually transmitted infections. https://www.who.int/reproductivehealth/publications/rtis/9789241502450/en/. Accessed 12 Apr 2021
Yooseph S, Kirkness EF, Tran TM, Harkins DM, Jones MB, Torralba MG, O’Connell E, Nutman TB, Doumbo S, Doumbo OK, Traore B, Crompton PD, Nelson KE (2015) Stool microbiota composition is associated with the prospective risk of Plasmodium falciparum infection. BMC Genom 16(1):631. https://doi.org/10.1186/s12864-015-1819-3
Zhang D, Li S, Wang N, Tan HY, Zhang Z, Feng Y (2020) The cross-talk between gut microbiota and lungs in common lung diseases. Front Microbiol 11:301. https://doi.org/10.3389/fmicb.2020.00301
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ulusan Bagci, O., Caner, A. The interaction of gut microbiota with parasitic protozoa. J Parasit Dis 46, 8–11 (2022). https://doi.org/10.1007/s12639-021-01443-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12639-021-01443-5