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Giardia intestinalis can interact, change its shape and internalize large particles and microorganisms

Published online by Cambridge University Press:  07 December 2020

Marlene Benchimol*
Affiliation:
UNIGRANRIO-Universidade do Grande Rio-Duque de Caxias-Rio de Janeiro, Rio de Janeiro, Brazil UFRJ-Universidade Federal do Rio de Janeiro-Instituto de Biofísica Carlos Chagas Filho-Laboratório de Ultraestrutura Celular Hertha Meyer, and Instituto Nacional de Ciência e Tecnologia-INBEB, Centro Nacional de Biologia Estrutural e Bioimagens-CENABIO, Rio de Janeiro, Brazil
*
Author for correspondence: Marlene Benchiumol, E-mail: [email protected]

Abstract

Giardia intestinalis is a parasitic protozoan that inhabits its vertebrate hosts' upper small intestine and is the most common cause of waterborne diarrhoea worldwide. Giardia trophozoites present few organelles, and among them, they possess peripheral vesicles (PVs), which are considered an endosomal–lysosomal system. All experimental procedures carried out until now indicate that Giardia ingests macromolecules by fluid-phase and receptor-mediated endocytic pathways. Still, there is no description concerning the interaction and ingestion of large materials. Here, we tested Giardia's capacity to interact with large particles; once, in vivo, it inhabits an environment with a microbiota. We tested protozoan interaction with yeasts, bacteria, latex beads, ferritin and albumin, in different times of interaction and used several microscopy techniques (light microscopy, scanning electron microscopy and transmission electron microscopy) to follow their fate. Giardia interacted with all of the materials we tested. Projections of the plasma membrane similar to pseudopods were seen. As albumin, small markers were found in the PVs while the larger materials were not seen there. Large vacuoles containing large latex beads were detected intracellularly. Thus, we observed that: (1) Giardia interacts with large materials; (2) Giardia can display an amoeboid shape and exhibit membrane projections when in contact with microorganisms and large inorganic materials; (3) the region of the exit of the ventral flagella is very active when in contact with large materials, although all cell surface also present activity in the interactions; (4) intracellular vacuoles, which are not the PVs, present ingested large beads.

Type
Research Article
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Abodeely, M, DuBois, KN, Hehl, A, Stefanic, S, Sajid, M, De Souza, W, Attias, M, Engel, JC, Hsieh, I, Fetter, RD and McKerrow, JH (2009) A contiguous compartment functions as endoplasmic reticulum and endosome/lysosome in Giardia lamblia. Eukaryotic Cell 8, 16651676.CrossRefGoogle ScholarPubMed
Acosta-Virgen, K, Chávez-Munguía, B, Talamás, LD, Guillén, DL, Martínez-Higuera, A, Lazcano, A, Martínez-Palomo, A and Espinosa-Cantellano, M (2018) Giardia lamblia: identification of peroxisomal-like proteins. Experimental Parasitology 191, 3643.CrossRefGoogle ScholarPubMed
Banerjee, S, Cui, J, Robbins, PW and Samuelson, J (2008) Use of Giardia, which appears to have a single nucleotide-sugar transporter for UDP-GlcNAc, to identify the UDP-Glc transporter of Entamoeba. Molecular Biochemical Parasitology 159, 4453.CrossRefGoogle ScholarPubMed
Bär, AK, Phukan, N, Pinheiro, J and Simoes-Barbosa, A (2015) The interplay of host, and parasitic protozoans at mucosal interfaces: implications for the outcomes of infections and diseases. PLoS Neglected Tropical Diseases 9, e0004176.CrossRefGoogle ScholarPubMed
Benchimol, M, Batista, C and De Souza, W (1990) Fibronectin – and – laminin mediated endocytic activity in the parasitic protozoa Trichomonas vaginalis and Tritrichomonas foetus. Journal of Submicroscopy and Cytology Pathology 22, 3945.Google ScholarPubMed
Dacks, JB and Field, MC (2007) Evolution of the eukaryotic membrane trafficking system: origin, tempo and mode. Journal of Cell Science 120, 29772985.CrossRefGoogle ScholarPubMed
Ebneter, JA, Heusser, SD, Schraner, EM, Hehl, AB and Faso, C (2016) Cyst wall-protein-1 is fundamental for Golgi-like organelle neogenesis and cyst wall biosynthesis in Giardia lamblia. Nature Communication 15, 13859.CrossRefGoogle Scholar
Faubert, G, Reiner, DS and Gillin, FD (1991) Giardia lamblia: regulation of secretory vesicle formation and loss of ability to reattach during encystation in vitro. Experimental Parasitology 72, 345354.CrossRefGoogle ScholarPubMed
Feely, DE and Dyer, JK (1987) Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trophozoites. Journal of Protozoology 34, 8083.CrossRefGoogle ScholarPubMed
Gaechter, V, Schraner, E, Wild, P and Hehl, AB (2008) The single dynamin family protein in the primitive protozoan Giardia lamblia is essential for stage conversion and endocytic transport. Traffic (Copenhagen, Denmark) 9, 5771.CrossRefGoogle ScholarPubMed
Hehl, AB and Marti, M (2004) Secretory protein trafficking in Giardia intestinalis. Molecular Microbiology 53, 1928.CrossRefGoogle ScholarPubMed
Hernandez, Y, Castillo, C, Roychowdhury, S, Hehl, A, Aley, SB and Das, S (2007) Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. International Journal for Parasitology 37, 2132.CrossRefGoogle ScholarPubMed
Kattenbach, WM, Pimenta, PFP, de Souza, W and Pinto da Silva, P (1991) Giardia duodenalis: a freeze-fracture, fracture-flip and cytochemistry study. Parasitology Research 77, 651658.CrossRefGoogle ScholarPubMed
Keister, DB (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 487488.CrossRefGoogle ScholarPubMed
Lanfredi-Rangel, A, Attias, M, Carvalho, TMU, Kattenbach, WM and De Souza, W (1998) The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and lysosomes. Journal Structural Biology 123, 225235.CrossRefGoogle ScholarPubMed
Lanfredi-Rangel, A, Kattenbach, WM, Diniz, JAJ and de Souza, W (1999) Trophozoites of Giardia lamblia may have a Golgi-like structure. FEMS Microbiology Letters 181, 245251.CrossRefGoogle ScholarPubMed
Lindmark, DG (1988) Giardia lamblia: localization of hydrolase activities in lysosome-like organelles of trophozoites. Experimental Parasitology 65, 141147.CrossRefGoogle ScholarPubMed
Luján, HD, Marotta, A, Mowatt, MR, Sciaky, N, Lippincottschwartz, J and Nash, TE (1995) Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. Journal of Biological Chemistry 270, 46124618.CrossRefGoogle ScholarPubMed
Makiuchi, T and Nozaki, T (2014) Highly divergent mitochondrion- related organelles in anaerobic parasitic protozoa. Biochimie 100, 317.CrossRefGoogle ScholarPubMed
Marie, C and Petri, WA Jr (2014) Regulation of virulence of Entamoeba histolytica. Annual Review of Microbiology 68, 493520.CrossRefGoogle ScholarPubMed
Marti, M, Li, Y, Schraner, EM, Wild, P, Kohler, P and Hehl, AB (2003) The secretory apparatus of an ancient eukaryote: protein sorting to separate export pathways occurs before formation of transient Golgi-like compartments. Molecular Biology of the Cell 14, 14331447.CrossRefGoogle ScholarPubMed
McCaffery, JM and Gillin, FD (1994) Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Experimental Parasitology 79, 220235.CrossRefGoogle ScholarPubMed
Midlej, V, Meinig, I, de Souza, W and Benchimol, M (2013) A new set of carbohydrate-positive vesicles in encysting Giardia lamblia. Protist 164, 261271.CrossRefGoogle ScholarPubMed
Midlej, V, Penha, L, Silva, R, de Souza, W and Benchimol, M (2016) Mitosomal chaperone modulation during the life cycle of the pathogenic protist Giardia intestinalis. European Journal of Cell Biology 95, 531542.CrossRefGoogle ScholarPubMed
Nemanic, PC, Owen, RL, Stevens, DP and Mueller, JC (1979) Ultrastructural observations on Giardiasis in a mouse model. II. Endosymbiosis and organelle distribution in Giardia muris and Giardia lamblia. Journal of Infectious Diseases 140, 222228.CrossRefGoogle Scholar
Orozco, E, Guarneros, G, Martinez-Palomo, A and Sánchez, T (1983) Entamoeba histolytica. Phagocytosis as a virulence factor. The Journal of Experimental Medicine 158, 15111521. https://doi.org/10.1084/jem.158.5.1511 .CrossRefGoogle ScholarPubMed
Pereira-Neves, A and Benchimol, M (2007) Phagocytosis by Trichomonas vaginalis: new insights. Biology of the Cell 99, 87101.CrossRefGoogle ScholarPubMed
Rivero, MR, Vranych, CV, Bisbal, M, Maletto, BA, Ropolo, AS and Touz, MC (2010) Adaptor protein 2 regulates receptor-mediated endocytosis and cyst formation in Giardia lamblia. Biochemical Journal 428, 3345.CrossRefGoogle ScholarPubMed
Rivero, MR, Miras, SL, Feliziani, C, Zamponi, N, Quiroga, R, Hayes, SF, Rópolo, AS and Touz, MC (2012) Vacuolar protein sorting receptor in Giardia lamblia. PLoS ONE 7, e43712.CrossRefGoogle ScholarPubMed
Sogayar, MIL and Gregorio, EA (1989) Uptake of bacteria by trophozoites of Giardia duodenalis (Say). Annals of Tropical Medicine and Parasitology 83, 6366.CrossRefGoogle Scholar
Stefanic, S, Morf, L, Kulangara, C, Regös, A, Sonda, S, Schraner, E, Spycher, C, Wild, P and Hehl, AB (2009) Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote. Journal of Cell Science 122, 28462856.CrossRefGoogle Scholar
Tachezy, J and Smid, O (2008) Mitosomes in parasitic protists. In Tachezy, J (ed.), Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Berlin: Springer-Verlag, pp. 201230.CrossRefGoogle Scholar
Tachezy, J, Sanchez, LB and Muller, M (2001) Mitochondrial type iron-sulfur cluster 15 assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Molecular Biology Evolution 18, 19191928.CrossRefGoogle Scholar
Tai, JH, Ong, SJ, Chang, SC and Su, HM (1993) Giardia virus enters Giardia lamblia WB trophozoite via endocytosis. Experimental Parasitology 76, 165174.CrossRefGoogle ScholarPubMed
Thiéry, JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal of Microscopy 6, 9871018.Google Scholar
Touz, MC, Kulakova, L and Nash, TE (2004) Adaptor protein complex 1 mediates the transport of lysosomal proteins from a Golgi-like organelle to peripheral vacuoles in the primitive eukaryote Giardia lamblia. Molecular Biology of the Cell 15, 30533060.CrossRefGoogle ScholarPubMed
Tovar, J, Fischer, A and Clark, CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Molecular Microbiology 32, 10131021.CrossRefGoogle ScholarPubMed
Tovar, J, León-Avila, G, Sánchez, LB, Sutak, R, Tachezy, J, van der Giezen, M, Hernández, M, Müller, M and Lucocq, JM (2003) Mitochondrial remnant organelles of Giardia Function in iron-sulphur protein maturation. Nature 426, 172176.CrossRefGoogle ScholarPubMed
Wampfler, PB, Tosevski, V, Nanni, P, Spycher, C and Hehl, AB (2014) Proteomics of secretory and endocytic organelles in Giardia lamblia. PLoS ONE 9, e94089.CrossRefGoogle ScholarPubMed
Zumthor, JP, Cernikova, L, Rout, S, Kaech, A, Faso, C and Hehl, AB (2016) Static clathrin assemblies at the peripheral vacuole-plasma membrane interface of the parasitic protozoan Giardia lamblia. PLoS Pathogens 12, e1005756.CrossRefGoogle ScholarPubMed