The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

Sarah M. Prostak, Kristyn A. Robinson, Margaret A. Titus, Lillian K. Fritz-Laylin

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Pages (from-to)1192-1205.e6
JournalCurrent Biology
Volume31
Issue number6
DOIs
StatePublished - Mar 22 2021

Bibliographical note

Funding Information:
We thank Tom Pollard, Harry Higgs, and Jessica Henty-Ridilla for feedback on Figure 2, as well as Madelaine Bartlett, Edgar Medina, Katrina Velle, and Samuel Lord for comments on the manuscript. We also thank Katrina Velle for assisting in deconvolution of confocal images, Edgar Medina for assisting with growth of Spizellomyces punctatus and Rhizoclosmatium globosum, and Terrell Redwood and Tatihana Beckford for assisting with data analysis. This material is based upon work supported by the Pew Charitable Trust (to L.K.F.-L.) and the National Institutes of Health (R01GM12291 to M.A.T.). S.M.P. organized and conducted the bioinformatic analysis of actin and actin regulatory proteins, designed and conducted the actin inhibition experiments and analysis, and wrote and edited the manuscript. K.A.R. provided several sets of images for analysis and edited the manuscript. M.A.T. conducted the myosin analyses and drafted and edited the manuscript. L.K.F.-L. designed experiments, analyzed data, and wrote and edited the manuscript. The authors declare no competing interests.

Funding Information:
We thank Tom Pollard, Harry Higgs, and Jessica Henty-Ridilla for feedback on Figure 2 , as well as Madelaine Bartlett, Edgar Medina, Katrina Velle, and Samuel Lord for comments on the manuscript. We also thank Katrina Velle for assisting in deconvolution of confocal images, Edgar Medina for assisting with growth of Spizellomyces punctatus and Rhizoclosmatium globosum, and Terrell Redwood and Tatihana Beckford for assisting with data analysis. This material is based upon work supported by the Pew Charitable Trust (to L.K.F.-L.) and the National Institutes of Health ( R01GM12291 to M.A.T.).

Publisher Copyright:
© 2021 The Author(s)

Keywords

  • actin
  • Batrachochytrium dendrobatidis
  • chytrid
  • cytoskeleton
  • development
  • evolution
  • formin
  • fungi
  • motility
  • myosin

PubMed: MeSH publication types

  • Journal Article

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