Actin guides filamentous rhizoid growth and morphogenesis in the zoosporic fungus Chytriomyces hyalinus

ABSTRACT

The advantage of filamentous growth to the fungal lifestyle is so great that it arose multiple times. Most zoosporic fungi from phylum Chytridiomycota exhibit a monocentric thallus form consisting of anucleate filamentous rhizoids that anchor reproductive sporangia to substrata and absorb nutrients. Actin function during polarized growth and cytokinesis is well documented across eukaryotes, but its role in sculpting nonhyphal, nonyeast fungal cells is unknown. We sought to provide a basis for comparing actin organization among major fungal lineages and to investigate the effects of actin disruption on morphogenesis in a monocentric thallus. Using fluorescence microscopy, we observed fixed, rhodamine phalloidin–stained actin in chemically fixed Chytriomyces hyalinus, exemplifying monocentric thallus development within the diverse, zoosporic phylum Chytridiomycota. We also compared rhizoid lengths and rhizoid branching of thalli incubated with the actin inhibitor latrunculin B to determine the effects of actin disruption on morphology. Actin was concentrated at the tips of growing rhizoids. Actin cables typically formed cortical, parallel arrays in hyphae, but in mature sporangia they were concentrated in a funnel-shaped array in the central region. Thalli treated with latrunculin B had shorter rhizoids with fewer branches than controls. In both hyphae and monocentric thalli, actin localization coincides with active, polarized growth and cytokinesis. Specific actin localization patterns are largely shared between monocentric species but differ significantly from patterns observed in hyphae. Actin integrity is critical for sustaining filamentous growth in all fungi.

KEYWORDS:

• Actin filaments
• actin inhibitor
• actin plaques
• chytrid
• Chytridiomycota
• hyphae
• latrunculin
• morphogenesis
• nuclear position
• zoosporogenesis

ACKNOWLEDGMENTS

The authors thank Dr. Joyce Longcore (University of Maine) for providing the C. hyalinus culture and Benoit Goulet for processing the culture at the Canadian Collection of Fungal Cultures. The authors also thank Justin Jubinville-Mah for conducting some of the thallus measurements. M.L.B. is supported by Discovery Grant RGPIN-2016–03746, National Science and Engineering Research Council of Canada. J.M.D. received research awards from the Mycological Society of America (Myron P. Backus Award) and the National Science and Engineering Research Council of Canada (Alexander Graham Bell Canada Graduate Scholarship).