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Evolutionarily diverse fungal zoospores show contrasting swimming patterns specific to ultrastructure

Abstract:
Zoosporic fungi, also called chytrids, produce single-celled motile spores with flagellar swimming tails (zoospores). These fungi are key components of aquatic food webs, acting as pathogens, saprotrophs, and prey. Little is known about the swimming behavior of fungal zoospores, a crucial factor governing dispersal, biogeographical range, ecological function, and infection dynamics. Here, we track the swimming patterns of zoospores from 12 evolutionarily divergent species of zoosporic fungi from across seven orders of the Chytridiomycota and the Blastocladiomycota. We report two major swimming patterns that correlate with the cytoskeletal ultrastructure of these zoospores. Specifically, we show that species without major cytoplasmic tubulin components swim in a circular fashion, while species with prominent cytoplasmic tubulin structures swim in a pattern akin to a random walk (move-stop-redirect-move). We confirm cytoskeletal architecture by performing fluorescence confocal microscopy across all 12 species. We then treat representative species with variant swimming behaviors and cytoplasmic-cytoskeletal arrangements with tubulin-stabilizing (Taxol) and depolymerizing (nocodazole) pharmacological compounds. We observed that when treating the “random walk” species with nocodazole, their swimming behavior changed to a circular-swimming pattern. Confocal imaging of the nocodazole-treated zoospores demonstrates that these cells maintain flagellum tubulin structures but lack their characteristic cytoplasmic tubulin structures. Our data demonstrate that the capability of zoospores to perform “complex” random-walk movement is linked to the presence of prominent cytoplasmic tubulin structures and suggest a link between cytology, sensory systems, and swimming behavior in a diversity of zoosporic fungi.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1016/j.cub.2024.08.016

Authors

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Institution:
University of Oxford
Division:
MPLS
Department:
Biology
Role:
Author
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Institution:
University of Oxford
Division:
MPLS
Department:
Biology
Oxford college:
Merton College
Role:
Author
ORCID:
0000-0002-9692-0973


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Funder identifier:
https://ror.org/00k4n6c32
Grant:
101022101
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Funder identifier:
https://ror.org/01cmst727


Publisher:
Cell Press
Journal:
Current Biology More from this journal
Volume:
34
Issue:
19
Pages:
p4567-4576.e3
Place of publication:
England
Publication date:
2024-09-11
Acceptance date:
2024-08-13
DOI:
EISSN:
1879-0445
ISSN:
0960-9822
Pmid:
39265568


Language:
English
Keywords:
Pubs id:
2032380
Local pid:
pubs:2032380
Deposit date:
2024-10-24
ARK identifier:

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