A hidden battle in the dirt: soil amoebae interactions withParacoccidioidesspp

Author:

Albuquerque PatríciaORCID,Nicola André Moraes,Magnabosco Diogo Almeida Gomes,Derengowski Lorena da Silveira,Crisóstomo Luana Soares,Xavier Luciano Costa Gomes,de Oliveira Frazão Stefânia,Guilhelmelli Fernanda,de Oliveira Marco Antônio,Hurtado Fabián Andrés,de Melo Teixeira Marcus,Guimaraes Allan J.,Paes Hugo Costa,Bagagli Eduardo,Felipe Maria Sueli Soares,Casadevall Arturo,Silva-Pereira Ildinete

Abstract

AbstractParacoccidioidesspp. are thermodimorphic pathogenic fungi endemic to Latin America. Predation is believed to drive the evolution of virulence for soil saprophytes. We evaluated the presence of environmental amoeboid predators in soil from armadillo burrows whereParacoccidioideshad been previously detected and tested if interaction ofParacoccidioideswith amoebae increased fungal virulence. Nematodes, ciliates and amoebae – all potential predators of fungi – grew in cultures from soil samples. Microscopical observation and ITS sequencing identified the amoebae asAcanthamoebaspp,Allovahlkampfia spelaeaandVermamoeba vermiformis. These three amoebae efficiently ingested, killed and digestedParacoccidioidesspp. yeast cells, as did laboratory-adapted axenicAcanthamoeba castellanii. Sequential co-cultivation ofParacoccidioideswithA. castellaniiselected for phenotypical traits related to survival of the fungus within a natural predator as well as in murine macrophages and in vivo (Galleria mellonellaand mice). This increase in virulence is linked to the accumulation of cell wall alpha-glucans, polysaccharides that masks recognition of fungal molecular patterns by host pattern recognition receptors. Altogether, our results indicate thatParacoccidioidesinhabits a complex environment with multiple amoeboid predators that can exert selective pressure to guide the evolution of virulence traits.

Publisher

Cold Spring Harbor Laboratory

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