Abstract
Cells from across the eukaryotic tree use actin polymer networks for a wide variety of functions, including endocytosis, cytokinesis, and cell migration. Despite this functional conservation, the actin cytoskeleton has undergone significant diversification, highlighted by the differences in the actin networks of mammalian cells and yeast. Chytrid fungi diverged before the emergence of the Dikarya (multicellular fungi and yeast) and therefore provide a unique opportunity to study actin cytoskeletal evolution. Chytrids have two life stages: zoospore cells that can swim with a flagellum and sessile sporangial cells that, like multicellular fungi, are encased in a chitinous cell wall. Here, we show that zoospores of the amphibian-killing chytrid Batrachochytrium dendrobatidis (Bd) build dynamic actin structures resembling those of animal cells, including an actin cortex, pseudopods, and filopodia-like spikes. In contrast, Bd sporangia assemble perinuclear actin shells and actin patches similar to those of yeast. The use of specific small-molecule inhibitors indicate that nearly all of Bd's actin structures are dynamic and use distinct nucleators: although pseudopods and actin patches are Arp2/3 dependent, the actin cortex appears formin dependent and actin spikes require both nucleators. Our analysis of multiple chytrid genomes reveals actin regulators and myosin motors found in animals, but not dikaryotic fungi, as well as fungal-specific components. The presence of animal- and yeast-like actin cytoskeletal components in the genome combined with the intermediate actin phenotypes in Bd suggests that the simplicity of the yeast cytoskeleton may be due to evolutionary loss.
Highlights
Actin participates in nearly every essential eukaryotic cell function, including endocytosis, intracellular trafficking, cell migration, and cytokinesis in many species
Actin polymerization is largely regulated by controlling the initiation of new actin polymers—a process called ‘‘actin nucleation.’’ Actin is nucleated by two main systems: the Arp2/3 complex and formin family proteins, both of which were likely present in the last common eukaryotic ancestor.[3]
We find that both the regulatory networks and actin structures of Batrachochytrium dendrobatidis (Bd) are intermediate in complexity between animals and Dikarya, suggesting that the streamlined actin networks of common model fungi are a result of secondary evolutionary loss of actin network components
Summary
Actin participates in nearly every essential eukaryotic cell function, including endocytosis, intracellular trafficking, cell migration, and cytokinesis in many species. Eukaryotic cells employ a sophisticated network of actin regulatory proteins to spatially and temporally control these diverse functions.[1] How these complex actin regulatory networks evolved and diversified remain key questions in both evolutionary and cell biology. We use chytrids—early-diverging fungi that still share important features of animal cells lost in yeast and other fungi2—as a system to explore the evolution of the actin cytoskeleton. Using a combination of genomics and fluorescence microscopy, we show that chytrid fungi have an actin cytoskeleton that combines features of animal cells and yeast. The Arp2/3 complex primarily builds actin branches along the side of existing actin filaments,[1] formins assemble unbranched filament networks through processive addition of actin monomers by their formin homology 2 (FH2) domains.[1,4]
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