Toxicity of Potential Fungal Defense Proteins towards the Fungivorous Nematodes Aphelenchus avenae and Bursaphelenchus okinawaensis

Tayyrov, Annageldi; Schmieder, Stefanie S.; Bleuler-Martinez, Silvia; Plaza, David Fernando; Künzler, Markus

doi:10.1128/aem.02051-18

Cited by 24 publications

(20 citation statements)

References 58 publications

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“…When feeding on germlings or hyphal filaments, P. aurantium penetrated the fungal cell wall, invaded the hyphae, and fed exclusively on the cytoplasmic content, indicating that the fungal cell wall primarily represents a barrier of rather low nutritional value. Hyphal perforation and cytoplasmic feeding have also been described for fungivorous nematodes which pierce the fungal cell wall and induce specific fungal defense mechanisms made up of lectins and anti‐nutritional proteins (Bleuler‐Martinez et al, ; Tayyrov et al, ). Adapting the feeding mode between phagocytosis to ‘ruphocytic’ invasion is, to our knowledge, an unprecedented predatory strategy on fungi.…”

Section: Discussionmentioning

confidence: 82%

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

Radosa

Ferling

Sprague

et al. 2019

Environmental Microbiology

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Summary Size and diverse morphologies pose a primary challenge for phagocytes such as innate immune cells and predatory amoebae when encountering fungal prey. Although filamentous fungi can escape phagocytic killing by pure physical constraints, unicellular spores and yeasts can mask molecular surface patterns or arrest phagocytic processing. Here, we show that the fungivorous amoeba Protostelium aurantium was able to adjust its killing and feeding mechanisms to these different cell shapes. Yeast‐like fungi from the major fungal groups of basidiomycetes and ascomycetes were readily internalized by phagocytosis, except for the human pathogen Candida albicans whose mannoprotein coat was essential to escape recognition by the amoeba. Dormant spores of the filamentous fungus Aspergillus fumigatus also remained unrecognized, but swelling and the onset of germination induced internalization and intracellular killing by the amoeba. Mature hyphae of A. fumigatus were mostly attacked from the hyphal tip and killed by an actin‐mediated invasion of fungal filaments. Our results demonstrate that predatory pressure imposed by amoebae in natural environments selects for distinct survival strategies in yeast and filamentous fungi but commonly targets the fungal cell wall as a crucial molecular pattern associated to prey and pathogens.

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Section: Discussionmentioning

confidence: 82%

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

Radosa

Ferling

Sprague

et al. 2019

Environmental Microbiology

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“…In order to protect themselves against predation, fungi have evolved various defense mechanisms (Kunzler, 2018). In addition to physical defense (Gomez and Nosanchuk, 2003;Latge, 2007) or chemical defense by secondary metabolites (Rohlfs and Churchill, 2011;Spiteller, 2015;Keller, 2019), fungi rely on chemical defense mediated by proteins and peptides (Sabotic et al, 2016;Tayyrov et al, 2018). Several fungal defense proteins, biotin-binding protein (Bleuler-Martinez et al, 2012),including lectins (Bleuler-Martinez et al, 2011), protease inhibitors (Renko et al, 2010),pore-forming proteins (Mancheno et al, 2010), and ribotoxins (Lacadena et al, 2007;Tayyrov et al, 2019a) have been characterized.…”

Section: Introductionmentioning

confidence: 99%

Cytoplasmic Lipases—A Novel Class of Fungal Defense Proteins Against Nematodes

Tayyrov

Wei

Fetz

et al. 2021

Front. Fungal Biol.

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Fungi are an attractive food source for predators such as fungivorous nematodes. Several fungal defense proteins and their protective mechanisms against nematodes have been described. Many of these proteins are lectins which are stored in the cytoplasm of the fungal cells and bind to specific glycan epitopes in the digestive tract of the nematode upon ingestion. Here, we studied two novel nematotoxic proteins with lipase domains from the model mushroom Coprinopsis cinerea. These cytoplasmically localized proteins were found to be induced in the vegetative mycelium of C. cinerea upon challenge with fungivorous nematode Aphelenchus avenae. The proteins showed nematotoxicity when heterologously expressed in E. coli and fed to several bacterivorous nematodes. Site-specific mutagenesis of predicted catalytic residues eliminated the in-vitro lipase activity of the proteins and significantly reduced their nematotoxicity, indicating the importance of the lipase activity for the nematotoxicity of these proteins. Our results suggest that cytoplasmic lipases constitute a novel class of fungal defense proteins against predatory nematodes. These findings improve our understanding of fungal defense mechanisms against predators and may find applications in the control of parasitic nematodes in agriculture and medicine.

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“…In the fungal prey–nematode predator relationship, just like other types of prey–predator relationships, the fungal prey can develop resistance mechanisms against nematode predation. One type of fungal prey defense is the production and secretion of toxic secondary metabolites and toxic proteins [ 18 ]. For example, the model mushroom Coprinopsis cinerea produces a toxic substance on its mycelial surface that can kill nematodes upon contact [ 19 ].…”

Section: Antagonistic Interactionsmentioning

confidence: 99%

“…One type of fungal prey defense is the production and secretion of toxic secondary metabolites and toxic proteins [18]. For example, the model mushroom Coprinopsis cinerea produces a toxic substance on its mycelial surface that can kill nematodes upon contact [19].…”

Section: Nematodes Feeding On and Antagonizing Fungimentioning

confidence: 99%

Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture

Zhang

et al. 2020

JoF

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Fungi and nematodes are among the most abundant organisms in soil habitats. They provide essential ecosystem services and play crucial roles for maintaining the stability of food-webs and for facilitating nutrient cycling. As two of the very abundant groups of organisms, fungi and nematodes interact with each other in multiple ways. Here in this review, we provide a broad framework of interactions between fungi and nematodes with an emphasis on those that impact crops and agriculture ecosystems. We describe the diversity and evolution of fungi that closely interact with nematodes, including food fungi for nematodes as well as fungi that feed on nematodes. Among the nematophagous fungi, those that produce specialized nematode-trapping devices are especially interesting, and a great deal is known about their diversity, evolution, and molecular mechanisms of interactions with nematodes. Some of the fungi and nematodes are significant pathogens and pests to crops. We summarize the ecological and molecular mechanisms identified so far that impact, either directly or indirectly, the interactions among phytopathogenic fungi, phytopathogenic nematodes, and crop plants. The potential applications of our understanding to controlling phytophagous nematodes and soilborne fungal pathogens in agricultural fields are discussed.

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Toxicity of Potential Fungal Defense Proteins towards the Fungivorous Nematodes Aphelenchus avenae and Bursaphelenchus okinawaensis

Cited by 24 publications

References 58 publications

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

Cytoplasmic Lipases—A Novel Class of Fungal Defense Proteins Against Nematodes

Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture

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