A filamentous archaeal virus is enveloped inside the cell and released through pyramidal portals

Abstract

The majority of viruses infecting hyperthermophilic archaea display unique virion architectures and are evolutionarily unrelated to viruses of bacteria and eukaryotes. The lack of relationships to other known viruses suggests that the mechanisms of virus–host interaction in Archaea are also likely to be distinct. To gain insights into archaeal virus–host interactions, we studied the life cycle of the enveloped, ∼2-μm-long Sulfolobus islandicus filamentous virus (SIFV), a member of the family Lipothrixviridae infecting a hyperthermophilic and acidophilic archaeon Saccharolobus islandicus LAL14/1. Using dual-axis electron tomography and convolutional neural network analysis, we characterize the life cycle of SIFV and show that the virions, which are nearly two times longer than the host cell diameter, are assembled in the cell cytoplasm, forming twisted virion bundles organized on a nonperfect hexagonal lattice. Remarkably, our results indicate that envelopment of the helical nucleocapsids takes place inside the cell rather than by budding as in the case of most other known enveloped viruses. The mature virions are released from the cell through large (up to 220 nm in diameter), six-sided pyramidal portals, which are built from multiple copies of a single 89-amino-acid-long viral protein gp43. The overexpression of this protein in Escherichia coli leads to pyramid formation in the bacterial membrane. Collectively, our results provide insights into the assembly and release of enveloped filamentous viruses and illuminate the evolution of virus–host interactions in Archaea.

Selective lipid recruitment by an archaeal DPANN symbiont from its host

“…antarcticus selectively acquires specific lipid species from its host. These observations match with the lipid uptake behavior noted for archaeal viruses 42 – 45 . For instance, the Sulfolobus filamentous virus 1 selectively acquired lipids from its host Sulfolobus shibatae for survial 44 .…”

Selective lipid recruitment by an archaeal DPANN symbiont from its host

“…antarcticus selectively acquires specific lipid species from its host. These observations match with the lipid uptake behavior noted for archaeal viruses 42,43,44,45 . For instance, the Sulfolobus filamentous virus 1 selectively acquired lipids from its host Sulfolobus shibatae for survial 44 .…”

Isolation of archaeal viruses with lipid membrane from Tengchong acidic hot springs

“…The lipid archaeol is less than 1% in the host membrane but reaches over 70% of lipids in the viral envelope. Thus, like other filamentous viruses AFV1, SFV1, and SIFV which selectively acquired archaeol or GDGT-0 from the pool of host lipids ( Wang et al, 2019 ; Baquero et al, 2021a ; Han et al, 2022 ), the lipids are incorporated into the SIFV3 envelope in a highly selective manner. The lipid compositions of the spindle-shaped virus STSV3 and STSV4 were slightly different from that of their host membrane.…”

“…For instance, the major membrane lipid composition of SIFV3 is substantially different from that of the host and the dominant lipid species in the viral membrane is archaeol. Similarly, the icosahedral virus SPV1 with inner membrane, the spindle-shaped viruses SSV1 and Sulfolobus monocaudavirus 1 (SMV1) with possible termini lipids, and the filamentous viruses (Acidianus filamentous virus 1 [AFV1], SFV1 and SIFV) with outside envelope could selectively acquire archaeol or GDGT-0 from the pool of host lipids ( Quemin et al, 2015 ; Kasson et al, 2017 ; Liu et al, 2018 ; Wang et al, 2019 ; Baquero et al, 2021a ; Han et al, 2022 ). To date, the mechanism of membrane lipid selection is still not be clearly explained.…”

“…However, the lipid composition of some Sulfolobus viral envelopes has been found to be quantitatively very different from that of the host membranes, even if the membrane lipids of all archaeal viruses are derived from the host lipid pool. For instance, Sulfolobus filamentous virus 1 (SFV1) and Sulfolobus islandicus filamentous virus (SIFV) were shown to selectively acquire host membrane lipids GDGT-0 (glycerol dibiphytanyl glycerol tetraether) or archaeol ( Liu et al, 2018 ; Baquero et al, 2021a ), yet the archaeol and GDGT-0 account for a small proportion of lipids in the host membrane and the dominant lipid species are tetraether lipids carrying four cyclopentane rings (GDGT-4). The mechanism of membrane lipid selection in viruses, however, has yet to be largely explored.…”