Structure and Replication Cycle of a Virus Infecting Climate-modulating Alga

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2024 Apr 10

PMID 38598627

Authors

Miroslav Homola

Carina R Buttner

Tibor Fuzik

Pavel Krepelka

Radka Holbova

Jiri Novacek

Marten L Chaillet

Jakub Zak

Danyil Grybchuk

Friedrich Forster

William H Wilson

Declan C Schroeder

Pavel Plevka

Affiliations

Soon will be listed here.

Abstract

The globally distributed marine alga has cooling effect on the Earth's climate. The population density of is restricted by viruses, including virus 201 (EhV-201). Despite the impact of viruses on the climate, there is limited information about their structure and replication. Here, we show that the dsDNA genome inside the EhV-201 virion is protected by an inner membrane, capsid, and outer membrane. EhV-201 virions infect by using fivefold vertices to bind to and fuse the virus' inner membrane with the cell plasma membrane. Progeny virions assemble in the cytoplasm at the surface of endoplasmic reticulum-derived membrane segments. Genome packaging initiates synchronously with the capsid assembly and completes through an aperture in the forming capsid. The genome-filled capsids acquire an outer membrane by budding into intracellular vesicles. EhV-201 infection induces a loss of surface protective layers from cells, which enables the continuous release of virions by exocytosis.

Citing Articles

Stability of a surrogate African swine fever-like algal virus in corn- and soybean-based feed ingredients during extended storage and digestion processes.

Shurson G, Ramirez-Camba C, Urriola P, Schroeder D Front Vet Sci. 2024; 11:1498977.

PMID: 39664890 PMC: 11631853. DOI: 10.3389/fvets.2024.1498977.

References

Hernaez B, Guerra M, Salas M, Andres G . African Swine Fever Virus Undergoes Outer Envelope Disruption, Capsid Disassembly and Inner Envelope Fusion before Core Release from Multivesicular Endosomes. PLoS Pathog. 2016; 12(4):e1005595. PMC: 4844166. DOI: 10.1371/journal.ppat.1005595. View

Mastronarde D, Held S . Automated tilt series alignment and tomographic reconstruction in IMOD. J Struct Biol. 2016; 197(2):102-113. PMC: 5247408. DOI: 10.1016/j.jsb.2016.07.011. View

Rybicka K . Glycosomes (protein-glycogen complex) in the canine heart. Ultrastructure, histochemistry and changes induced by acidic treatment. Virchows Arch B Cell Pathol Incl Mol Pathol. 1979; 30(3):335-47. DOI: 10.1007/BF02889112. View

Okamoto K, Miyazaki N, Reddy H, Hantke M, Maia F, Larsson D . Cryo-EM structure of a Marseilleviridae virus particle reveals a large internal microassembly. Virology. 2018; 516:239-245. DOI: 10.1016/j.virol.2018.01.021. View

Rybicka K . Simultaneous demonstration of glycogen and protein in glycosomes of cardiac tissue. J Histochem Cytochem. 1981; 29(1):4-8. DOI: 10.1177/29.1.6162880. View

Chinchar V, Yu K, Jancovich J . The molecular biology of frog virus 3 and other iridoviruses infecting cold-blooded vertebrates. Viruses. 2011; 3(10):1959-85. PMC: 3205390. DOI: 10.3390/v3101959. View

Rose S, Fulton J, Brown C, Natale F, Van Mooy B, Bidle K . Isolation and characterization of lipid rafts in Emiliania huxleyi: a role for membrane microdomains in host-virus interactions. Environ Microbiol. 2013; 16(4):1150-66. DOI: 10.1111/1462-2920.12357. View

Himes B, Zhang P . emClarity: software for high-resolution cryo-electron tomography and subtomogram averaging. Nat Methods. 2018; 15(11):955-961. PMC: 6281437. DOI: 10.1038/s41592-018-0167-z. View

Vincent F, Sheyn U, Porat Z, Schatz D, Vardi A . Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise. Proc Natl Acad Sci U S A. 2021; 118(11). PMC: 7980383. DOI: 10.1073/pnas.2021586118. View

10.

Gendrault J, Steffan A, Bingen A, KIRN A . Penetration and uncoating of frog virus 3 (FV3) in cultured rat Kupffer cells. Virology. 1981; 112(2):375-84. DOI: 10.1016/0042-6822(81)90284-1. View

11.

Han G, Gable K, Yan L, Allen M, Wilson W, Moitra P . Expression of a novel marine viral single-chain serine palmitoyltransferase and construction of yeast and mammalian single-chain chimera. J Biol Chem. 2006; 281(52):39935-42. DOI: 10.1074/jbc.M609365200. View

12.

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View

13.

Xiao C, Kuznetsov Y, Sun S, Hafenstein S, Kostyuchenko V, Chipman P . Structural studies of the giant mimivirus. PLoS Biol. 2009; 7(4):e92. PMC: 2671561. DOI: 10.1371/journal.pbio.1000092. View

14.

Sturgess J, Mitranic M, Moscarello M . Extraction of glycoproteins during tissue preparation for electron microscopy. J Microsc. 1978; 114(1):101-5. DOI: 10.1111/j.1365-2818.1978.tb00120.x. View

15.

Mackinder L, Worthy C, Biggi G, Hall M, Ryan K, Varsani A . A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. J Gen Virol. 2009; 90(Pt 9):2306-16. DOI: 10.1099/vir.0.011635-0. View

16.

Yan X, Olson N, Van Etten J, Bergoin M, Rossmann M, Baker T . Structure and assembly of large lipid-containing dsDNA viruses. Nat Struct Biol. 2000; 7(2):101-3. PMC: 4167659. DOI: 10.1038/72360. View

17.

Zhang K . Gctf: Real-time CTF determination and correction. J Struct Biol. 2015; 193(1):1-12. PMC: 4711343. DOI: 10.1016/j.jsb.2015.11.003. View

18.

Vardi A, Haramaty L, Van Mooy B, Fredricks H, Kimmance S, Larsen A . Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc Natl Acad Sci U S A. 2012; 109(47):19327-32. PMC: 3511156. DOI: 10.1073/pnas.1208895109. View

19.

Guillard R, Ryther J . Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol. 1962; 8:229-39. DOI: 10.1139/m62-029. View

20.

Schramm B, Krijnse Locker J . Cytoplasmic organization of POXvirus DNA replication. Traffic. 2005; 6(10):839-46. DOI: 10.1111/j.1600-0854.2005.00324.x. View