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A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli

View ORCID ProfileErica A. Birkholz, View ORCID ProfileThomas G. Laughlin, View ORCID ProfileSergey Suslov, View ORCID ProfileEmily Armbruster, Jina Lee, View ORCID ProfileJohannes Wittmann, View ORCID ProfileKevin D. Corbett, View ORCID ProfileElizabeth Villa, View ORCID ProfileJoe Pogliano
doi: https://doi.org/10.1101/2021.10.25.465362
Erica A. Birkholz
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
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  • ORCID record for Erica A. Birkholz
Thomas G. Laughlin
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
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  • ORCID record for Thomas G. Laughlin
Sergey Suslov
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
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Emily Armbruster
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
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Jina Lee
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
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Johannes Wittmann
2Leibniz Institute DSMZ–German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany
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Kevin D. Corbett
3Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla CA
4Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla CA
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Elizabeth Villa
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
5Howard Hughes Medical Institute, University of California, San Diego, La Jolla, CA
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Joe Pogliano
1Division of Biological Sciences, University of California, San Diego, La Jolla, CA
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  • For correspondence: jpogliano@ucsd.edu
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Abstract

Vortex-like arrays of cytoskeletal filaments that drive cytoplasmic streaming and nucleus rotation have been identified in eukaryotes, but similar structures have not been described in prokaryotes. The only known example of a rotating intracellular body in prokaryotic cells occurs when nucleus-forming jumbo phages infect Pseudomonas. During infection, a bipolar spindle of PhuZ filaments drives intracellular rotation of the phage nucleus, a key aspect of the replication cycle. Here we show the E. coli jumbo phage Goslar assembles a phage nucleus surrounded by an array of PhuZ filaments resembling a vortex instead of a bipolar spindle. Expression of mutant PhuZ strongly reduces Goslar phage nucleus rotation, demonstrating that the PhuZ cytoskeletal vortex is necessary for rotating the phage nucleus. While vortex-like cytoskeletal arrays are important in eukaryotes, this work identifies the first known example of a coherent assembly of filaments into a vortex-like structure driving intracellular rotation within the prokaryotic cytoplasm.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 26, 2021.
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A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli
Erica A. Birkholz, Thomas G. Laughlin, Sergey Suslov, Emily Armbruster, Jina Lee, Johannes Wittmann, Kevin D. Corbett, Elizabeth Villa, Joe Pogliano
bioRxiv 2021.10.25.465362; doi: https://doi.org/10.1101/2021.10.25.465362
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A Cytoskeletal Vortex Drives Phage Nucleus Rotation During Jumbo Phage Replication in E. coli
Erica A. Birkholz, Thomas G. Laughlin, Sergey Suslov, Emily Armbruster, Jina Lee, Johannes Wittmann, Kevin D. Corbett, Elizabeth Villa, Joe Pogliano
bioRxiv 2021.10.25.465362; doi: https://doi.org/10.1101/2021.10.25.465362

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