The Cytoskeleton Architecture of Algivorous Protoplast Feeders (Viridiraptoridae, Rhizaria) Indicates Actin-Guided Perforation of Prey Cell Walls

Busch, Anna; Hess, Sebastian

doi:10.1016/j.protis.2016.10.004

Cited by 12 publications

(20 citation statements)

References 78 publications

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“…Adapting the feeding mode between phagocytosis to ‘ruphocytic’ invasion is, to our knowledge, an unprecedented predatory strategy on fungi. A similar actin‐guided, invasive predation has also been recently described for the amoeboflagellate Viridiraptor invadens when feeding on the protoplasm of multicellular algae (Busch and Hess, ). The distant relationship between the two organisms, however, as well as scattered earlier reports on fungal predation by vampyrellid amoebae (Chakraborty and Old, ), suggest that invading filamentous organisms might be an effective hunting strategy spread across different groups of protists.…”

Section: Discussionmentioning

confidence: 99%

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: 99%

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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“…The cell wall dissolution is confined to a narrow elliptical zone, which results in removal of a lid-like cell wall disc (Figure 1B). This perforation pattern appears to be defined by a transient F-actin-rich domain, the lysopodium 2 (Figure 1C). As revealed by scanning electron microscopy, Orciraptor degrades both main structural components of the plant-like algal cell wall, (i) crystalline cellulose microfibrils and (ii) gel-like pectic substances (Figure 1D).…”

Section: Resultsmentioning

confidence: 99%

Comparative transcriptomics reveals the molecular toolkit used by an algivorous protist for cell wall perforation

Gerbracht

Harding

Simpson

et al. 2021

Preprint

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Microbial eukaryotes display a stunning diversity of feeding strategies, ranging from generalist predators to highly specialised parasites. The unicellular protoplast feeders represent a fascinating mechanistic intermediate, as they penetrate other eukaryotic cells (algae, fungi) like some parasites, but then devour their cell contents by phagocytosis. Besides prey recognition and attachment, this complex behaviour involves the local, pre-phagocytotic dissolution of the prey cell wall, which results in well-defined perforations of species-specific size and structure. Yet, the molecular processes that enable protoplast feeders to overcome cell walls of diverse biochemical composition remain unknown. We used the flagellate Orciraptor agilis (Viridiraptoridae, Rhizaria) as a model protoplast feeder, and applied differential gene expression analysis to examine its penetration of green algal cell walls. Besides distinct expression changes that reflect major cellular processes (e.g. locomotion, cell division), we found lytic carbohydrate-active enzymes that are highly expressed and upregulated during the attack on the alga. A putative endocellulase (family GH5_5) with a secretion signal is most prominent, and a potential key factor for cell wall dissolution. Other candidate enzymes (e.g. lytic polysaccharide monooxygenases) belong to families that are largely uncharacterised, emphasising the potential of non-fungal micro-eukaryotes for enzyme exploration. Unexpectedly, we discovered various chitin-related factors that point to an unknown chitin metabolism in Orciraptor, potentially also involved in the feeding process. Our findings provide first molecular insights into an important microbial feeding behaviour, and new directions for cell biology research on non-model eukaryotes.

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“…Similar feeding mechanisms to that of S. perlucida were observed for the putative amoebozoan Rhizamoeba schnepfii and the cercozoan flagellate Cryothecomonas longipes, both of which penetrate marine planktonic diatoms in the girdle region and subsequently phagocytose the cell contents (Kühn, 1997;Schnepf & Kühn, 2000). In the distantly related viridiraptorid amoeboflagellates (Viridiraptoridae, Rhizaria), which perforate the cell walls of zygnematophycean green algae, the actomyosin system seems to be crucial for the removal of an excised disc of the algal cell wall (Orciraptor agilis) and infiltration of the cell (Viridiraptor invadens) (Busch & Hess, 2017). These processes typically start with the insertion of a minute pseudopodium, which then enlarges and (very likely) exerts the required force.…”

Section: Discussionmentioning

confidence: 99%

Description of the marine predator Sericomyxa perlucida gen. et sp. nov., a cultivated representative of the deepest branching lineage of vampyrellid amoebae (Vampyrellida, Rhizaria)

Simpson

Hess

2021

J Eukaryotic Microbiology

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The Cytoskeleton Architecture of Algivorous Protoplast Feeders (Viridiraptoridae, Rhizaria) Indicates Actin-Guided Perforation of Prey Cell Walls

Cited by 12 publications

References 78 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

Comparative transcriptomics reveals the molecular toolkit used by an algivorous protist for cell wall perforation

Description of the marine predator Sericomyxa perlucida gen. et sp. nov., a cultivated representative of the deepest branching lineage of vampyrellid amoebae (Vampyrellida, Rhizaria)

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