The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis
Abstract
:1. Introduction
2. Early Studies on the Interaction of Fungi and Amoeba
3. Correspondence of Virulence Factors for Animals and Amoeba
3.1. C. neoformans
3.2. Aspergillus spp.
3.3. Candida spp.
3.4. Other Pathogenic Fungi
4. Amoeba and Fungal Dimorphism
5. Considerations, Caveats and Unsolved Questions
5.1. Insights Drawn Primarily from a Few Amoeba and Fungal Species
5.2. Ascendancy in Fungal–Amoeba Interactions
5.3. Animal Pathogenic Fungi–Amoeba Interactions in Context
5.4. Fungal–Amoeba Interaction and Susceptibility to Antifungals
6. A Restatement of the Amoeboid Predator—Animal Virulence Hypothesis
Author Contributions
Funding
Conflicts of Interest
References
- Robert, V.A.; Casadevall, A. Vertebrate endothermy restricts most fungi as potential pathogens. J. Infect. Dis. 2009, 200, 1623–1626. [Google Scholar] [CrossRef] [PubMed]
- Bergman, A.; Casadevall, A. Mammalian endothermy optimally restricts fungi and metabolic costs. mBio 2010, 1. [Google Scholar] [CrossRef] [PubMed]
- Casadevall, A. Fungi and the rise of mammals. PLoS Pathog. 2012, 8, e1002808. [Google Scholar] [CrossRef]
- Desjardins, C.A.; Giamberardino, C.; Sykes, S.M.; Yu, C.H.; Tenor, J.L.; Chen, Y.; Yang, T.; Jones, A.M.; Sun, S.; Haverkamp, M.R.; et al. Population genomics and the evolution of virulence in the fungal pathogen Cryptococcus neoformans. Genome Res. 2017, 27, 1207–1219. [Google Scholar] [CrossRef] [PubMed]
- Steenbergen, J.N.; Shuman, H.A.; Casadevall, A. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc. Natl. Acad. Sci. USA 2001, 18, 15245–15250. [Google Scholar] [CrossRef] [PubMed]
- Steenbergen, J.N.; Nosanchuk, J.D.; Malliaris, S.D.; Casadevall, A. Interaction of Blastomyces dermatitidis, Sporothrix schenckii, and Histoplasma capsulatum with Acanthamoeba castellanii. Infect. Immun. 2004, 72, 3478–3488. [Google Scholar] [CrossRef] [PubMed]
- Malliaris, S.D.; Steenbergen, J.N.; Casadevall, A. Cryptococcus neoformans var. gattii can exploit Acanthamoeba castellanii for growth. Med. Mycol. 2004, 42, 149–158. [Google Scholar]
- Van Waeyenberghe, L.; Bare, J.; Pasmans, F.; Claeys, M.; Bert, W.; Haesebrouck, F.; Houf, K.; Martel, A. Interaction of Aspergillus fumigatus conidia with Acanthamoeba castellanii parallels macrophage-fungus interactions. Environ. Microbiol. Rep. 2013, 5, 819–824. [Google Scholar] [CrossRef]
- Bidochka, M.J.; Clark, D.C.; Lewis, M.W.; Keyhani, N.O. Could insect phagocytic avoidance by entomogenous fungi have evolved via selection against soil amoeboid predators? Microbiology 2010, 156 Pt 7, 2164–2171. [Google Scholar] [CrossRef] [Green Version]
- Allen, P.G.; Dawidowicz, E.A. Phagocytosis in Acanthamoeba: I. A mannose receptor is responsible for the binding and phagocytosis of yeast. J. Cell. Physiol. 1990, 145, 508–513. [Google Scholar] [CrossRef]
- Allen, P.G.; Dawidowicz, E.A. Phagocytosis in Acanthamoeba: II. Soluble and insoluble mannose-rich ligands stimulate phosphoinositide metabolism. J. Cell. Physiol. 1990, 145, 514–521. [Google Scholar] [CrossRef]
- Molmeret, M.; Horn, M.; Wagner, M.; Santic, M.; Abu, K.Y. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 2005, 71, 20–28. [Google Scholar] [CrossRef] [PubMed]
- Harb, O.S.; Gao, L.Y.; Abu Kwaik, Y. From protozoa to mammalian cells: A new paradigm in the life cycle of intracellular bacterial pathogens. Environ. Microbiol. 2000, 2, 251–265. [Google Scholar] [CrossRef] [PubMed]
- Hilbi, H.; Weber, S.S.; Ragaz, C.; Nyfeler, Y.; Urwyler, S. Environmental predators as models for bacterial pathogenesis. Environ. Microbiol. 2007, 9, 563–575. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mylonakis, E.; Casadevall, A.; Ausubel, F.M. Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog. 2007, 3, e101. [Google Scholar] [CrossRef] [PubMed]
- Davies, B.; Chattings, L.S.; Edwards, S.W. Superoxide generation during phagocytosis by Acanthamoeba castellanii: Similarities to the respiratory burst of immune phagocytes. Microbiology 1991, 137, 705–710. [Google Scholar] [CrossRef]
- Broderick, N.A. A common origin for immunity and digestion. Front. Immunol. 2015, 6, 72. [Google Scholar] [CrossRef]
- Novohradska, S.; Ferling, I.; Hillmann, F. Exploring Virulence Determinants of Filamentous Fungal Pathogens through Interactions with Soil Amoebae. Front. Cell. Infect. Microbiol. 2017, 7, 497. [Google Scholar] [CrossRef]
- Balczun, C.; Scheid, P.L. Free-Living Amoebae as Hosts for and Vectors of Intracellular Microorganisms with Public Health Significance. Viruses 2017, 9, 65. [Google Scholar] [CrossRef]
- Guimaraes, A.J.; Gomes, K.X.; Cortines, J.R.; Peralta, J.M.; Peralta, R.H. Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence. Microbiol. Res. 2016, 193, 30–38. [Google Scholar] [CrossRef]
- Castellani, A. An amoeba growing in cultures of a yeast. J. Trop. Med. Hyg. 1931, 33, 188–191. [Google Scholar]
- Castellani, A. Phagocytic and destructive action of Hartmanella castellanii (Amoeba castellanii) on pathogenic encapsulated yeast-like fungus Torulopsis neoformans (Cryptococcus neoformans). Ann. Inst. Pasteur 1955, 89, 1–7. [Google Scholar]
- Nero, L.C.; Tarver, M.G.; Hedrick, L.R. Growth of Acanthomoeba castellani with the yeast Torulopsis famata. J. Bacteriol. 1964, 87, 220–225. [Google Scholar] [PubMed]
- Bunting, L.A.; Neilson, J.B.; Bulmer, G.S. Cryptococcus neoformans: Gastronomic delight of a soil ameba. Sabouraudia 1979, 17, 225–232. [Google Scholar] [CrossRef] [PubMed]
- Neilson, J.B.; Fromtling, R.A.; Bulmer, G.S. Pseudohyphal forms of Cryptococcus neoformans: Decreased survival in vivo. Mycopathologia 1981, 73, 57–59. [Google Scholar] [CrossRef] [PubMed]
- Ruiz, A.; Neilson, J.B.; Bulmer, G.S. Control of Cryptococcus neoformans in nature by biotic factors. Sabouraudia 1982, 20, 21–29. [Google Scholar] [CrossRef] [PubMed]
- Bowen, I.D.C.; Coakley, W.T.; James, C.J. The digestion of Saccharomyces cerevisiase by Acanthamoeba castellanii. Protoplasma 1979, 98, 63–71. [Google Scholar] [CrossRef]
- Heal, O. Soil fungi as food for amoebae. In Soil Organisms; North Holland: Amsterdam, The Netherlands, 1963; pp. 289–297. [Google Scholar]
- Esser, R.; Ridings, W.; Sobers, E. (Eds.) Ingestion of fungus spores by protozoa. Proc. Soil Crop Sci. Soc. Fla. 1975, 34, 206–208. [Google Scholar]
- Chakraborty, S.; Old, K.; Warcup, J. Amoebae from a take-all suppressive soil which feed on Gaeumannomyces graminis tritici and other soil fungi. Soil Biol. Biochem. 1983, 15, 17–24. [Google Scholar] [CrossRef]
- Old, K.; Darbyshire, J. Soil fungi as food for giant amoebae. Soil Biol. Biochem. 1978, 10, 93–100. [Google Scholar] [CrossRef]
- Old, K. Perforation and lysis of fungal spores by soil amoebae. Ann. Appl. Biol. 1978, 89, 128–131. [Google Scholar] [CrossRef]
- Zaragoza, O.; Chrisman, C.J.; Castelli, M.V.; Frases, S.; Cuenca-Estrella, M.; Rodriguez-Tudela, J.L.; Casadevall, A. Capsule enlargement in Cryptococcus neoformans confers resistance to oxidative stress suggesting a mechanism for intracellular survival. Cell. Microbiol. 2008, 10, 2043–2057. [Google Scholar] [CrossRef]
- Nielsen, K.; Cox, G.M.; Litvintseva, A.P.; Mylonakis, E.; Malliaris, S.D.; Benjamin, D.K., Jr.; Giles, S.S.; Mitchell, T.G.; Casadevall, A.; Perfect, J.R.; et al. Cryptococcus neoformans {alpha} strains preferentially disseminate to the central nervous system during coinfection. Infect. Immun. 2005, 73, 4922–4933. [Google Scholar] [CrossRef] [PubMed]
- Cox, G.M.; Mukherjee, J.; Cole, G.T.; Casadevall, A.; Perfect, J.R. Urease as a virulence factor in experimental cryptococcosis. Infect. Immun. 2000, 68, 443–448. [Google Scholar] [CrossRef]
- Fu, M.S.; Coelho, C.; De Leon-Rodriguez, C.M.; Rossi, D.C.P.; Camacho, E.; Jung, E.H.; Kulkarni, M.; Casadevall, A. Cryptococcus neoformans urease affects the outcome of intracellular pathogenesis by modulating phagolysosomal pH. PLoS Pathog. 2018, 14, e1007144. [Google Scholar] [CrossRef] [PubMed]
- Guimaraes, A.J.; Frases, S.; Cordero, R.J.; Nimrichter, L.; Casadevall, A.; Nosanchuk, J.D. Cryptococcus neoformans responds to mannitol by increasing capsule size in vitro and in vivo. Cell. Microbiol. 2010, 12, 740–753. [Google Scholar] [CrossRef]
- Chatuverdi, V.; Flynn, T.; Niehaus, W.G.; Wong, B. Stress tolerance and pathogenic potential of a mannitol mutant of Cryptococcus neoformans. Microbiology 1996, 142, 937–943. [Google Scholar]
- Hamilton, A.J.; Holdom, M.D. Antioxidant systems in the pathogenic fungi of man and their role in virulence. Med. Mycol. 1999, 37, 375–389. [Google Scholar] [CrossRef] [Green Version]
- Olszewski, M.A.; Noverr, M.C.; Chen, G.H.; Toews, G.B.; Cox, G.M.; Perfect, J.R.; Huffnagle, G.B. Urease expression by Cryptococcus neoformans promotes microvascular sequestration, thereby enhancing central nervous system invasion. Am. J. Pathol. 2004, 164, 1761–1771. [Google Scholar] [CrossRef]
- Shi, M.; Li, S.S.; Zheng, C.; Kim, K.S.; Zhou, H.; Kubes, P.; Mody, C.H. Real-time imaging of trapping and urease-dependent transmigration of Cryptococcus in the brain. J. Clin. Investig. 2010, 120, 1683–1693. [Google Scholar] [CrossRef]
- Neal, L.M.; Xing, E.; Xu, J.; Kolbe, J.L.; Osterholzer, J.J.; Segal, B.M.; Williamson, P.R.; Olszewski, M.A. CD4(+) T Cells Orchestrate Lethal Immune Pathology despite Fungal Clearance during Cryptococcus neoformans Meningoencephalitis. mBio 2017, 8. [Google Scholar] [CrossRef] [PubMed]
- Pirofski, L.A.; Casadevall, A. Immune-Mediated Damage Completes the Parabola: Cryptococcus neoformans Pathogenesis Can Reflect the Outcome of a Weak or Strong Immune Response. mBio 2017, 8. [Google Scholar] [CrossRef]
- Panackal, A.A.; Williamson, K.C.; van de Beek, D.; Boulware, D.R.; Williamson, P.R. Fighting the Monster: Applying the Host Damage Framework to Human Central Nervous System Infections. mBio 2016, 7, e01906-15. [Google Scholar] [CrossRef] [PubMed]
- Fu, M.S.; Casadevall, A. Divalent metal cations potentiate the predatory capacity of amoeba for Cryptococcus neoformans. Appl. Environ. Microbiol. 2017. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Solache, M.A.; Izquierdo-Garcia, D.; Smith, C.; Bergman, A.; Casadevall, A. Fungal virulence in a lepidopteran model is an emergent property with deterministic features. mBio 2013, 4, e00100-13. [Google Scholar] [CrossRef]
- Chrisman, C.J.; Albuquerque, P.; Guimaraes, A.J.; Nieves, E.; Casadevall, A. Phospholipids trigger Cryptococcus neoformans capsule enlargement during interactions with amoebae and macrophages. PLoS Pathog. 2011, 7, e1002047. [Google Scholar] [CrossRef]
- Ma, H.; Croudace, J.E.; Lammas, D.A.; May, R.C. Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 2006, 16, 2156–2160. [Google Scholar] [CrossRef]
- Alvarez, M.; Casadevall, A. Cell-to-cell spread and massive vacuole formation after Cryptococcus neoformans infection of murine macrophages. BMC Immunol. 2007, 8, 16. [Google Scholar] [CrossRef]
- Chrisman, C.J.; Alvarez, M.; Casadevall, A. Phagocytosis of Cryptococcus neoformans by, and nonlytic exocytosis from, Acanthamoeba castellanii. Appl. Environ. Microbiol. 2010, 76, 6056–6062. [Google Scholar] [CrossRef]
- Watkins, R.A.; Andrews, A.; Wynn, C.; Barisch, C.; King, J.S.; Johnston, S.A. Cryptococcus neoformans Escape From Dictyostelium Amoeba by Both WASH-Mediated Constitutive Exocytosis and Vomocytosis. Front. Cell. Infect. Microbiol. 2018, 8, 108. [Google Scholar] [CrossRef]
- Carnell, M.; Zech, T.; Calaminus, S.D.; Ura, S.; Hagedorn, M.; Johnston, S.A.; May, R.C.; Soldati, T.; Machesky, L.M.; Insall, R.H. Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis. J. Cell Biol. 2011, 193, 831–839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodrigues, M.L.; Nimrichter, L.; Oliveira, D.L.; Frases, S.; Miranda, K.; Zaragoza, O.; Alvarez, M.; Nakouzi, A.; Feldmesser, M.; Casadevall, A. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot. Cell 2007, 6, 48–59. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, D.L.; Freire-de-Lima, C.G.; Nosanchuk, J.D.; Casadevall, A.; Rodrigues, M.L.; Nimrichter, L. Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect. Immun. 2010, 78, 1601–1609. [Google Scholar] [CrossRef] [PubMed]
- Rizzo, J.; Albuquerque, P.C.; Wolf, J.M.; Nascimento, R.; Pereira, M.D.; Nosanchuk, J.D.; Rodrigues, M.L. Analysis of multiple components involved in the interaction between Cryptococcus neoformans and Acanthamoeba castellanii. Fungal Biol. 2017, 121, 602–614. [Google Scholar] [CrossRef] [PubMed]
- Madu, U.L.; Ogundeji, A.O.; Pohl, C.H.; Albertyn, J.; Sebolai, O.M. Elucidation of the Role of 3-Hydroxy Fatty Acids in Cryptococcus-amoeba Interactions. Front. Microbiol. 2017, 8, 765. [Google Scholar] [CrossRef] [PubMed]
- Steenbergen, J.N.; Nosanchuk, J.D.; Malliaris, S.D.; Casadevall, A. Cryptococcus neoformans virulence is enhanced after intracellular growth in the genetically malleable host Dictyostelium discoideum. Infect. Immun. 2003, 71, 4862–4872. [Google Scholar] [CrossRef]
- Frager, S.Z.; Chrisman, C.J.; Shakked, R.; Casadevall, A. Paramecium species ingest and kill the cells of the human pathogenic fungus Cryptococcus neoformans. Med. Mycol. 2010, 48, 775–779. [Google Scholar] [CrossRef]
- Yli-Pirila, T.; Kusnetsov, J.; Haatainen, S.; Hanninen, M.; Jalava, P.; Reiman, M.; Seuri, M.; Hirvonen, M.R.; Nevalainen, A. Amoebae and other protozoa in material samples from moisture-damaged buildings. Environ. Res. 2004, 96, 250–256. [Google Scholar] [CrossRef]
- Yli-Pirila, T.; Kusnetsov, J.; Hirvonen, M.R.; Seuri, M.; Nevalainen, A. Effects of amoebae on the growth of microbes isolated from moisture-damaged buildings. Can. J. Microbiol. 2006, 52, 383–390. [Google Scholar] [CrossRef]
- Maisonneuve, E.; Cateau, E.; Kaaki, S.; Rodier, M.H. Vermamoeba vermiformis-Aspergillus fumigatus relationships and comparison with other phagocytic cells. Parasitol. Res. 2016, 115, 4097–4105. [Google Scholar] [CrossRef]
- Hillmann, F.; Novohradska, S.; Mattern, D.J.; Forberger, T.; Heinekamp, T.; Westermann, M.; Winckler, T.; Brakhage, A.A. Virulence determinants of the human pathogenic fungus Aspergillus fumigatus protect against soil amoeba predation. Environ. Microbiol. 2015, 17, 2858–2869. [Google Scholar] [CrossRef] [PubMed]
- Arico-Muendel, C.; Centrella, P.A.; Contonio, B.D.; Morgan, B.A.; O’Donovan, G.; Paradise, C.L.; Skinner, S.R.; Sluboski, B.; Svendsen, J.L.; White, K.F.; et al. Antiparasitic activities of novel, orally available fumagillin analogs. Bioorgan. Med. Chem. Lett. 2009, 19, 5128–5131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guruceaga, X.; Ezpeleta, G.; Mayayo, E.; Sueiro-Olivares, M.; Abad-Diaz-De-Cerio, A.; Aguirre Urizar, J.M.; Liu, H.G.; Wiemann, P.; Bok, J.W.; Filler, S.G.; et al. A possible role for fumagillin in cellular damage during host infection by Aspergillus fumigatus. Virulence 2018, 9, 1548–1561. [Google Scholar] [CrossRef]
- Hobson, R.P. The effects of diffusates from the spores of Aspergillus fumigatus and A. terreus on human neutrophils, Naegleria gruberi and Acanthamoeba castellanii. Med. Mycol. 2000, 38, 133–141. [Google Scholar] [CrossRef] [PubMed]
- Bertout, S.; Badoc, C.; Mallie, M.; Giaimis, J.; Bastide, J.M. Spore diffusate isolated from some strains of Aspergillus fumigatus inhibits phagocytosis by murine alveolar macrophages. FEMS Immunol. Med. Microbiol. 2002, 33, 101–106. [Google Scholar] [CrossRef] [PubMed]
- Geib, E.; Gressler, M.; Viediernikova, I.; Hillmann, F.; Jacobsen, I.D.; Nietzsche, S.; Hertweck, C.; Brock, M. A Non-canonical Melanin Biosynthesis Pathway Protects Aspergillus terreus Conidia from Environmental Stress. Cell Chem. Biol. 2016, 23, 587–597. [Google Scholar] [CrossRef] [PubMed]
- Dao, A.H.; Robinson, D.P.; Wong, S.W. Frequency of Entamoeba gingivalis in human gingival scrapings. Am. J. Clin. Pathol. 1983, 80, 380–383. [Google Scholar] [CrossRef]
- Vanessa, B.; Virginie, M.; Nathalie, Q.; Marie-Helene, R.; Christine, I. Hartmannella vermiformis can promote proliferation of Candida spp. in tap-water. Water Res. 2012, 46, 5707–5714. [Google Scholar] [CrossRef]
- Koller, B.; Schramm, C.; Siebert, S.; Triebel, J.; Deland, E.; Pfefferkorn, A.M.; Rickerts, V.; Thewes, S. Dictyostelium discoideum as a Novel Host System to Study the Interaction between Phagocytes and Yeasts. Front. Microbiol. 2016, 7, 1665. [Google Scholar] [CrossRef]
- Levrat, P.; Pussard, M.; Steinberg, C.; Alabouvette, C. Regulation of Fusarium oxysporum populations introducied into soils: The amoebal predation hypothesis. FEMS Microbiol. Ecol. 1991, 86, 123–130. [Google Scholar] [CrossRef]
- Siddiqui, R.; Lakhundi, S.; Khan, N.A. Interactions of Pseudomonas aeruginosa and Corynebacterium spp. with non-phagocytic brain microvascular endothelial cells and phagocytic Acanthamoeba castellanii. Parasitol. Res. 2015, 114, 2349–2356. [Google Scholar] [CrossRef] [PubMed]
- Nunes, T.E.; Brazil, N.T.; Fuentefria, A.M.; Rott, M.B. Acanthamoeba and Fusarium interactions: A possible problem in keratitis. Acta Trop. 2016, 157, 102–107. [Google Scholar] [CrossRef] [PubMed]
- Cateau, E.; Hechard, Y.; Fernandes, B.; Rodier, M.H. Free living amoebae could enhance Fusarium oxysporum growth. Fungal Ecol. 2004, 8, 12–17. [Google Scholar] [CrossRef]
- Joseph, J.; Chaurasia, S.; Sharma, S. Case Report: Corneal Coinfection with Fungus and Amoeba: Report of Two Patients and Literature Review. Am. J. Trop. Med. Hyg. 2018, 99, 805–808. [Google Scholar] [CrossRef] [PubMed]
- Magditch, D.A.; Liu, T.B.; Xue, C.; Idnurm, A. DNA mutations mediate microevolution between host-adapted forms of the pathogenic fungus Cryptococcus neoformans. PLoS Pathog. 2012, 8, e1002936. [Google Scholar] [CrossRef]
- Lin, J.; Idnurm, A.; Lin, X. Morphology and its underlying genetic regulation impact the interaction between Cryptococcus neoformans and its hosts. Med. Mycol. 2015, 53, 493–504. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Neilson, J.B.; Ivey, M.H.; Bulmer, G.S. Cryptococcus neoformans: Pseudohyphal forms surviving culture with Acanthamoeba polyphaga. Infect. Immun. 1978, 20, 262–266. [Google Scholar]
- Chakraborty, S.; Old, K. Mycophagous soil amoeba: Interactions with three plant pathogenic fungi. Soil Biol. Biochem. 1982, 14, 247–255. [Google Scholar] [CrossRef]
- Chakraborty, S.; Old, K.M. Ultrastructure and Description of a Fungus-Feeding Amoeba, Trichamoeba mycophaga n. sp.(Amoebidae, Amoebea), from Australia. J. Protozool. 1986, 33, 564–569. [Google Scholar] [CrossRef]
- Bleuler-Martinez, S.; Butschi, A.; Garbani, M.; Walti, M.A.; Wohlschlager, T.; Potthoff, E.; Sabotiĉ, J.; Pohleven, J.; Lüthy, P.; Hengartner, M.O.; et al. A lectin-mediated resistance of higher fungi against predators and parasites. Mol. Ecol. 2011, 20, 3056–3070. [Google Scholar] [CrossRef]
- Corsaro, D.; Kohsler, M.; Wylezich, C.; Venditti, D.; Walochnik, J.; Michel, R. New insights from molecular phylogenetics of amoebophagous fungi (Zoopagomycota, Zoopagales). Parasitol. Res. 2018, 117, 157–167. [Google Scholar] [CrossRef] [PubMed]
- Vohnik, M.; Burdikova, Z.; Albrechtova, J.; Vosatka, M. Testate amoebae (Arcellinida and Euglyphida) vs. Ericoid mycorrhizal and DSE fungi: A possible novel interaction in the mycorrhizosphere of ericaceous plants? Microb. Ecol. 2009, 57, 203–214. [Google Scholar] [CrossRef] [PubMed]
- De Sousa, J.R.P.; Goncalves, V.N.; de Holanda, R.A.; Santos, D.A.; Bueloni, C.; Costa, A.O.; Petry, M.V.; Rosa, C.A.; Rosa, L.H. Pathogenic potential of environmental resident fungi from ornithogenic soils of Antarctica. Fungal Biol. 2017, 121, 991–1000. [Google Scholar] [CrossRef] [PubMed]
- McClelland, E.E.; Nicola, A.M.; Prados-Rosales, R.; Casadevall, A. Ab binding alters gene expression in Cryptococcus neoformans and directly modulates fungal metabolism. J. Clin. Investig. 2010, 120, 1355–1361. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Casadevall, A.; Pirofski, L.A. Accidental virulence, cryptic pathogenesis, martians, lost hosts, and the pathogenicity of environmental microbes. Eukaryot. Cell 2007, 6, 2169–2174. [Google Scholar] [CrossRef]
- Salah, I.B.; Ghigo, E.; Drancourt, M. Free-living amoebae, a training field for macrophage resistance of mycobacteria. Clin. Microbiol. Infect. 2009, 15, 894–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huws, S.A.; Morley, R.J.; Jones, M.V.; Brown, M.R.; Smith, A.W. Interactions of some common pathogenic bacteria with Acanthamoeba polyphaga. FEMS Microbiol. Lett. 2008, 282, 258–265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Greub, G.; Raoult, D. Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 2004, 17, 413–433. [Google Scholar] [CrossRef] [PubMed]
- Casadevall, A. The cards of virulence and the global virulome. Microbe 2007, 1, 359–364. [Google Scholar]
- Araujo Gde, S.; Fonseca, F.L.; Pontes, B.; Torres, A.; Cordero, R.J.; Zancope-Oliveira, R.M.; Casadevall, A.; Viana, N.B.; Nimrichter, L.; Rodrigues, M.L.; et al. Capsules from pathogenic and non-pathogenic Cryptococcus spp. manifest significant differences in structure and ability to protect against phagocytic cells. PLoS ONE 2012, 7, e29561. [Google Scholar] [CrossRef]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Casadevall, A.; Fu, M.S.; Guimaraes, A.J.; Albuquerque, P. The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis. J. Fungi 2019, 5, 10. https://doi.org/10.3390/jof5010010
Casadevall A, Fu MS, Guimaraes AJ, Albuquerque P. The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis. Journal of Fungi. 2019; 5(1):10. https://doi.org/10.3390/jof5010010
Chicago/Turabian StyleCasadevall, Arturo, Man Shun Fu, Allan J. Guimaraes, and Patricia Albuquerque. 2019. "The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis" Journal of Fungi 5, no. 1: 10. https://doi.org/10.3390/jof5010010
APA StyleCasadevall, A., Fu, M. S., Guimaraes, A. J., & Albuquerque, P. (2019). The ‘Amoeboid Predator-Fungal Animal Virulence’ Hypothesis. Journal of Fungi, 5(1), 10. https://doi.org/10.3390/jof5010010