Structure and replication cycle of a virus infecting climate-modulating alga Emiliania huxleyi

The globally distributed marine alga Emiliania huxleyi produces reflective
calcite disks (coccoliths) that increase the albedo of ocean water and
thus reduce the heat absorption in the ocean, which cools the Earth’s
climate. The population density of E. huxleyi is restricted by
Nucleocytoviricota viruses, including E. huxleyi virus 201 (EhV-201).
Despite the impact of E. huxleyi 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 decorated with numerous transmembrane proteins.
The virions are prone to deformation, and parts of their capsids deviate
from the icosahedral arrangement. EhV-201 virions infect E. huxleyi by
using their fivefold vertex to bind to a host cell and fuse the virus’s
inner membrane with the plasma membrane. Whereas the replication of
EhV-201 probably occurs in the nucleus, 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. Upon the completion of genome
packaging, the capsids change conformation, which enables them to acquire
an outer membrane by budding into intracellular vesicles. EhV-201
infection induces a loss of surface protective layers from E. huxleyi
cells, which allows the continuous release of virions by exocytosis. Our
results provide insight into how EhVs bypass the surface protective layers
of E. huxleyi and exploit the organelles of an infected cell for progeny
assembly.