Family: Adenoviridae

Genus: Siadenovirus

Distinguishing features

Siadenoviruses are serologically and phylogenetically distinct from members of the other adenovirus genera (Davison et al., 2000, Harrach et al., 2019). They have been identified in frog (Davison et al., 2000), birds (Zsivanovits et al., 2006, Wellehan et al., 2009, Kovács et al., 2010, Kovács and Benkő 2011, Joseph et al., 2014, Ballmann and Harrach 2016, Cassmann et al., 2019, Sutherland et al., 2019, Yang et al., 2019) (and GenBank accession MK695679) and tortoise (Rivera et al., 2009, Schumacher et al., 2012). The completely sequenced siadenoviruses have the shortest adenovirus genomes known to date. The genomic organization of siadenoviruses is also characteristic of the genus and different from that of other genera: the V and IX genes and homologues of the genes in mastadenovirus early regions E1, E3 and E4 are absent, and most siadenoviruses encode a sialidase that is not encoded by other adenoviruses  (Davison et al., 2000, Kovács and Benkő 2011). 

Virion

Morphology

The 3D fiber structures of turkey adenovirus 3 (TAdV-3; turkey haemorrhagic virus) and raptor adenovirus 1 (RAdV-1) have been established (Singh et al., 2015, Nguyen et al., 2016). 

Physicochemical and physical properties

See discussion under family properties. 

Nucleic acid

TAdV-3 was the first siadenovirus to be sequenced, from viral DNA extracted from the spleen of experimentally infected turkeys (Pitcovski et al., 1998). Frog adenovirus 1 (FrAdV-1) was the first siadenovirus to be sequenced from an isolated virus and the only amphibian adenovirus to have been sequenced to date (Davison et al., 2000). The RAdV-1 genome was fully sequenced using PCR amplification from tissue from an infected Harris’s hawk without virus isolation (Kovács and Benkő 2011). Recently, psittacine siadenoviruses have been sequenced (Athukorala et al., 2021) and novel species have been established to include these viruses: psittacine adenovirus 5 (PsAdV-5) from Pacific parrotlet, sun parakeet, cockatiel and budgerigar, and psittacine adenovirus 6 from another budgerigar (Gottdenker et al., 2019) (and GenBank Accession MK695679) belong to Psittacine siadenovirus D, while psittacine adenovirus 7 from little corella (Sutherland et al., 2019) belongs to Psittacine siadenovirus E. The siadenovirus genomes are the shortest adenovirus genomes known to date. The genomes with seemingly correctly sequenced genome ends are between 24,630 (gentoo penguin adenovirus 4) and 27,163 bp (PsAdV-5) (Lee et al., 2016, Sutherland et al., 2019) and have G+C contents of 34.23% (South Polar skua adenovirus 1) to 38.48% ( RAdV-1), and inverted terminal repeats (ITRs) of 26 (PsAdV-5) to 39 bp (TAdV-3) (Pitcovski et al., 1998). 

Proteins

See discussion under family properties. 

Lipids

None reported. 

Carbohydrates

See discussion under family properties. 

Genome organization and replication

The genomic organization of siadenoviruses is characteristic of the genus and different from that of other genera (Figure 2. Adenoviridae). The V and IX genes and homologues of the genes in mastadenovirus early regions E1, E3 and E4 are absent. There are only five ORFs potentially encoding novel proteins not encoded by members of other genera (Park et al., 2012). At the left end of the genome, the first putative gene encodes a protein that is related to sialidases (Davison et al., 2000). This gene is present in all siadenoviruses sequenced to date except the penguin siadenoviruses (Lee et al., 2016). However, the function of this protein is unknown. Adjacent to this gene is a novel ORF predicted to encode a highly hydrophobic protein (accordingly named “hydrophobic protein”) or another novel gene (ORF4) or both (overlapping). Gene E3 is named solely because of its position between the pVIII and fiber genes, but it is not homologous to any of the mastadenovirus E3 genes (or to any other known genes). The right end of the genome harbours ORF7 and ORF8 in all characterized siadenoviruses, and even one or two further genes (“hypothetical protein A” or ORF9 and “hypothetical protein B”) in some psittacine adenoviruses, e.g. PsAdV-2 (Athukorala et al., 2021) (and GenBank accession MZ562791). 

Most siadenoviruses have not been isolated and propagated. TAdV-3 can be propagated on transformed cell lines (MDTC-RP19 lymphoblastoid turkey cell line established from tumours induced by Marek’s disease virus (family Herpesviridae) in turkeys), and the gene expression profile of TAdV-3 has been analysed (Aboezz et al., 2019). FrAdV-1 can be propagated on the epithelial cell line TH-1 derived from box turtle (Terrapene carolina) heart cells. TAdV-3 uses sialic acid on N-linked glycoproteins as a cellular receptor (Mahsoub et al., 2020). 

Biology

The genus comprises eight species, most of which include several strains, but a growing number of novel and partially characterized AdVs also apparently belong to the genus. Members of current  species include FrAdV-1 and viruses detected in or isolated from birds: TAdV-3, RAdV-1, South Polar skua adenovirus 1, great tit adenovirus 1, chinstrap penguin adenovirus 2 and gentoo penguin adenovirus 4, and numerous psittacine siadenoviruses. FrAdV-1 was isolated from a northern leopard frog (on the TH-1 cell line), and TAdV-3 has been isolated from various galliformes (turkey, pheasant and chicken). RAdV-1 was detected by PCR in deceased captive raptors (Indian eagle-owl, Werreaux’s eagle-owl also known as the milky eagle owl, and Harris’s hawk). FrAdV-1 is not known to be pathogenic in frogs or any other animal. TAdV-3 is associated with specific diseases in various hosts (haemorrhagic enteritis in turkeys, marble spleen disease in pheasants and splenomegaly in chickens) (Palya et al., 2007). Psittacine adenovirus 2 seems to have an elevated pathogenicity for various psittacine birds (Psittaciformes) (Ballmann and Vidovszky 2013, Phalen et al., 2019, Yang et al., 2019). The single siadenovirus found in a tortoise, Sulawesi tortoise adenovirus 1, seems to be able to cross species barriers by infecting and killing different (captive) tortoise species (Rivera et al., 2009, Schumacher et al., 2012). 

Antigenicity

TAdV-3 has no common complement-fixing antigen with other adenoviruses isolated from birds and classified in the genera Aviadenovirus or Atadenovirus. 

Species demarcation criteria

Species designation depends on at least two of the following characteristics:

• Phylogenetic distance (>10–15%, based on distance matrix analysis of the DNA polymerase amino acid sequence)
• Host range
• Nucleotide composition
• Genome organization

Related, unclassified viruses

Virus names and virus abbreviations are not official ICTV designations. 

Many avian siadenoviruses have been detected only by partial sequencing, e.g. from psittacines: plum headed parakeet, umbrella cockatoo, etc. (Wellehan et al., 2009), budgerigar, cockatiel (Cassmann et al., 2019) and rainbow lorikeet (Chang et al., 2020). The phylogenetic relationships of these siadenoviruses, especially when partial sequences are available from different genes, remain to be established firmly, but several of these viruses may belong to the same species. Additional avian siadenoviruses have been detected in passerines (perching birds or songbirds, Passeriformes): great tit (Kovács et al., 2010), Gouldian finch (Joseph et al., 2014), long-tailed finch (Phalen et al., 2019) (the same virus also in zebra finch and double-barred finch), Eurasian blackcap (Rinder et al., 2020) and racing and fancy pigeons (Columbiformes) (Ballmann and Harrach 2016).