Sequential membrane- and protein-bound organelles compartmentalize genomes during phage infection

Armbruster, Emily G.; Rani, Phoolwanti; Lee, Jina; Klusch, Niklas; Hutchings, Joshua; Hoffman, Lizbeth Y.; Buschkaemper, Hannah; Enustun, Eray; Adler, Benjamin A.; Inlow, Koe; VanderWal, Arica R.; Hoffman, Madelynn Y.; Daksh, Daksh; Aindow, Ann; Deep, Amar; Rodriguez, Zaida K.; Morgan, Chase J.; Ghassemian, Majid; Laughlin, Thomas G.; Charles, Emeric; Cress, Brady F.; Savage, David F.; Doudna, Jennifer A.; Pogliano, Kit; Corbett, Kevin D.; Villa, Elizabeth; Pogliano, Joe

doi:10.1016/j.chom.2025.03.005

Sequential membrane- and protein-bound organelles compartmentalize genomes during phage infection

Journal Article · Mon Mar 31 00:00:00 EDT 2025 · Cell Host & Microbe

DOI:https://doi.org/10.1016/j.chom.2025.03.005· OSTI ID:2565632

Armbruster, Emily G. ^[1]; Rani, Phoolwanti ^[1]; Lee, Jina ^[1]; Klusch, Niklas ^[1]; Hutchings, Joshua ^[1]; Hoffman, Lizbeth Y. ^[1]; Buschkaemper, Hannah ^[2]; Enustun, Eray ^[1]; Adler, Benjamin A. ^[3]; Inlow, Koe ^[1]; VanderWal, Arica R. ^[1]; Hoffman, Madelynn Y. ^[1]; Daksh, Daksh ^[4]; Aindow, Ann ^[1]; Deep, Amar ^[1]; Rodriguez, Zaida K. ^[1]; Morgan, Chase J. ^[1]; Ghassemian, Majid ^[1]; Laughlin, Thomas G. ^[1]; Charles, Emeric ^[3] more »

Univ. of California, San Diego, CA (United States)
Univ. of California, San Diego, CA (United States); Ludwig Maximilian Univ. of Munich, Munich (Germany)
University of California, Berkeley, CA (United States)
National Institute of Science, Education and Research (NISER) (India)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Many eukaryotic viruses require membrane-bound compartments for replication, but no such organelles are known to be formed by prokaryotic viruses. Bacteriophages of the Chimalliviridae family sequester their genomes within a phage-generated organelle, the phage nucleus, which is enclosed by a lattice of the viral protein ChmA. We show that inhibiting phage nucleus formation arrests infections at an early stage in which the injected phage genome is enclosed within a membrane-bound early phage infection (EPI) vesicle. Early phage genes are expressed from the EPI vesicle, demonstrating its functionality as a prokaryotic, transcriptionally active, membrane-bound organelle. We also show that the phage nucleus is essential, with genome replication beginning after the injected DNA is transferred from the EPI vesicle to the phage nucleus. Our results show that Chimalliviridae require two sophisticated subcellular compartments of distinct compositions and functions that facilitate successive stages of the viral life cycle.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2565632

Journal Information:: Cell Host & Microbe, Journal Name: Cell Host & Microbe Journal Issue: 4 Vol. 33; ISSN 1931-3128

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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