Adnaviria
Adnaviria is a realm of viruses that includes archaeal viruses that have a filamentous virion and a linear, double-stranded DNA genome. Their genomes exist in A-form and encode a dimeric major capsid protein that contains the SIRV2 fold, an alpha-helix bundle with four helices. Adnavirians infect hyperthermophilic, thermoacidophilic, and methanotrophic archaea. They can be found worldwide, though some are concentrated in extreme geothermal environments. Their A-DNA genome is formed by interactions between pre-genomic B-DNA and the MCP and may be an adaptation to extremely high temperatures.
The virion of viruses in the realm consists of the genome encased in capsid proteins to form a helical nucleoprotein complex. For some adnavirians, this helix is surrounded by a lipid membrane called an envelope. Some contain an additional protein layer between the nucleoprotein helix and the envelope. Complete virions are long and thin and may be flexible or stiff like a rod. In general, enveloped adnavirians are more flexible than non-enveloped ones. At both ends of the virion are protrusions involved in host recognition. Virions are assembled and enveloped in the host cell's cytoplasm.
Adnavirians may have infected the last archaeal common ancestor. In general, they have no genetic relation to viruses outside the realm. How adnavirians interact with their hosts is not well understood, but it is known that they are lytic viruses, leaving their host through ruptures in the cell's external membrane. Adnavirians use a variety of methods to replicate their genomes and rely on host machinery for transcription. They were first discovered in the 1980s, and the realm Adnaviria was established in 2021 after cryogenic electron microscopy showed that they shared their A-DNA, MCP, and general virion structure.
Classification
Adnaviria is monotypic down to the rank of its sole class, Tokiviricetes, which has three orders. This is shown hereafter:- Realm: Adnaviria
- * Kingdom: Zilligvirae
- ** Phylum: Taleaviricota
- *** Class: Tokiviricetes
- **** Order: Ligamenvirales, which contains chiyouviruses, lipothrixviruses, rudiviruses, and ungulaviruses
- **** Order: Maximonvirales, which contains ahmunviruses
- **** Order: Primavirales, which contains tristromaviruses
Characteristics
Genome
Viruses in Adnaviria have linear, double-stranded DNA genomes that range from about 17.6 to 41.5 kilobase pairs in length. The ends of their genomes contain inverted terminal repeats. Their genomes exist in A-form, also called A-DNA, a dehydrated version of the more typical B-form DNA. A-DNA has a compact right-handed helix with more base pairs per turn than B-DNA, and the base pairs in A-DNA are not perpendicular to the DNA's helix axis. The creation of genomic A-DNA is caused by an interaction with major capsid protein dimers, which, during virion assembly, interact with the phosphodiester bond DNA backbone to cover pre-genomic B-DNA to form a helical nucleoprotein complex that contains genomic A-DNA. The A-form genome may be an adaptation to allow DNA survival at extremely high temperatures.Major capsid protein
The nucleoprotein helix is composed of asymmetric units of two MCPs. For rudiviruses, this is homodimer, a molecule formed by the bonding of two identical MCPs. For other adnavirians, it is heterodimer, a molecule formed by the bonding of two different MCPs that are paralogous, i.e., the result of a gene duplication event. The MCPs of viruses in Adnaviria have a folded structure that contains an alpha-helix bundle that has four helices, called the SIRV2 fold, named after Sulfolobus islandicus rod-shaped [virus 2]. The four-helix bundle is found at the end of the protein, while the beginning of the protein has an extended alpha-helical arm that, when a part of MCP dimers, forms a closed claw-like shape that wraps tightly around the dsDNA genome to change it to A-form. Variations in the protein structure exist, but the same base structure is retained in all adnavirians. The genes that encode the MCP are the only genes found in all viruses in the realm.Structure
The extracellular body of adnavirians is filamentous, i.e. they are long, thin, and cylindrical. Virions are about 400–2,000 nanometers in length and 24–38nm in diameter. Lipothrixviruses and ungulaviruses have flexible virions in which the nucleoprotein helix is surrounded by a lipid envelope. Tristromaviruses likewise have flexible, enveloped virions with an additional protein sheath layer between the nucleoprotein complex and the envelope. The envelopes of the aforementioned families are derived from host diether and tetraether lipids. Rudviruses have stiff, non-enveloped, rod-like virions about 600–900 by 23 nm. Non-enveloped adnavirians are more rigid, while enveloped adnavirians are more flexible. At both ends of the virion, lipothrixviruses and ungulaviruses have mop- or claw-like structures connected to a collar, whereas rudiviruses and tristromaviruses have plugs at each end from which bundles of thin filaments emanate. These protrusions are usually genus-specific, and they are made of minor structural proteins and involved in host recognition. Ahmunvirus and chiyouvirus virions have not been studied.Replication
Most research on adnavirian replication has focused on rudiviruses, but it is known that adnavirians replicate through a variety of mechanisms. Rudiviruses encode a HUH-superfamily endonuclease, which is thought to initiate rolling circle replication by nicking dsDNA close to the hairpin at the end of the genome. For SIRV2, a rudivirus, replication occurs through a combination of strand-displacement, rolling-circle, and strand-coupled methods, which generates multimeric, highly branched intermediate molecules that resemble brushes. These intermediates are then processed into individual genomes. Acidianus filamentous virus 1, an ungulavirus, appears to start replication first by forming a D-loop, then progressing through a strand-displacement mechanism. Replication then ends with the help of recombination through the formation of loop-like structures.Classified adnavirians do not encode their own DNA polymerases, so replication is likely performed by host DNA polymerases. For rudiviruses, DNA polymerase B1 and a sliding clamp are involved in replication. Ahmunviruses encode homologs of the archaeo-eukaryotic primase and DNA polymerase sliding clamp, which likely are important during replication. Partial genomes of putative adnavirians that encode protein-primed family B DNA polymerases have been identified by metagenomics, suggesting more replication methods are used by adnavirians than what is currently known.
Interactions with hosts
Adnavirians are known to infect hyperthermophilic, thermoacidophilic, and methanotrophic archaea. Known and predicted hosts include thermophilic archaea of the orders Sulfolobales, Thermoproteales, and Candidatus Bathyarchaeales, all of which belong to the phylum Thermoproteota. Ahmunviruses infect anaerobic methanotrophic archaea of the class Candidatus Syntropharchaeia in the phylum Halobacteriota. Adnavirians can be found worldwide, though some, such as rudiviruses, are concentrated in extreme geothermal environments.How adnavirians interact with their hosts is poorly understood. Rudiviruses, tristromaviruses, and ungulaviruses recognize and bind to extracellular filaments during viral entry to the cell. For rudiviruses and tristromaviruses, these are type IV pili. After reaching the cell surface, rudiviruses virions disassemble, likely at the same time that viral DNA enters the host cell's cytoplasm. Once there, transcription of viral genes begins, starting with proteins that take over the host and defend against host immune systems, such as anti-CRISPR proteins to protect against CRISPR defense systems. Adnavirians do not encode their own RNA polymerases, so they rely on host transcription machinery. They do, however, encode proteins that regulate transcription.
Virion assembly and envelopment take place in the cytoplasm. Characterized adnavirians are lytic viruses, leaving the cell through ruptures in the cell's external membrane. Rudivirus and lipothrixvirus virions exit the cell through pyramidal portals commonly called virus-associated pyramids. VAPs are made of a small virus-encoded protein and are formed at the same time as virions. At the end of infection, once VAPs reach a certain size, their triangular surfaces come apart like flower petals. These form large holes in the cell envelope through which virions and other contents of the cytoplasm are released into the extracellular environment. Tristromaviruses appear to use a different method of lysis during which cells are sliced open without any defined structures on the cell envelope.