Family: Adenoviridae

Genus: Aviadenovirus

Distinguishing features

Aviadenoviruses are serologically distinct from members of the other adenovirus genera and seem to infect only birds. Aviadenovirus genomes are considerably larger than those of mastadenoviruses. The genomic organization of aviadenoviruses is also different from that of adenoviruses in other genera (Chiocca et al., 1996, Grgić et al., 2011, Kaján et al., 2012, Marek et al., 2014b). 

Virion

Morphology

Except for fowl aviadenoviruses, which contain two fibers per vertex, with considerably different lengths in the case of fowl adenovirus 1 (FAdV-1), the morphology and number of fibers per vertex has not yet been determined. The genomes of FAdV-1, fowl adenovirus 4 (FAdV-4), fowl adenovirus 10 (FAdV-10), turkey adenovirus 1 (TAdV-1), turkey adenovirus 5 (TAdV-5), duck adenovirus 3 (DAdV-3), duck adenovirus 4 (DAdV-4), pigeon adenovirus 1 (PiAdV-1), pigeon adenovirus 2 (PiAdV-2), goose adenovirus 4 (GoAdV-4), psittacine adenovirus 1 (PsAdV-1), psittacine adenovirus 4 (PsAdV-4) and white-eyed parakeet adenovirus 2 have two fiber genes (Zhang et al., 2016, Huang et al., 2020). Other aviadenoviruses (fowl adenovirus 2,  fowl adenovirus 3,  fowl adenovirus 5, fowl adenovirus 6,  fowl adenovirus 7,  fowl adenovirus 8a,  fowl adenovirus 8b,  fowl adenovirus 9, fowl adenovirus 11, duck adenovirus 2 (DAdV-2), crane adenovirus 1 and turkey adenovirus 4) have only one (https://sites.google.com/site/adenoseq/). 

Physicochemical and physical properties

See discussion under family properties. 

Nucleic acid

Aviadenovirus genomes are longer than those of mastadenoviruses. Genomes range between 38,694 bp (PsAdV-1) (Milani et al., 2018) and 45,810 (FAdV-4), and the G+C content of the (almost) complete sequences of aviadenovirus genomes varies between 34.16% (crane adenovirus 1) (Mukai et al., 2019) and 66.92% (TAdV-1). Inverted terminal repeats (ITRs) are between 39 (GoAdV-4) (Kaján et al., 2012) and 721 bp (DAdV-2) (Marek et al., 2014b). 

Proteins

See discussion under family properties. 

Lipids

None reported. 

Carbohydrates

See discussion under family properties. 

Genome organization and replication

The genomic organization of aviadenoviruses is different from that of other adenoviruses (Figure 2. Adenoviridae) (Chiocca et al., 1996, Davison et al., 2003b, Marek et al., 2014b, Milani et al., 2018). The genes of proteins V and IX, as well as genes in mastadenovirus early regions E1 and E3, are missing. The E4 region may have been translocated from its position in mastadenovirus genomes, resulting in the gene encoding dUTP pyrophosphatase (dUTPase, not present in every mastadenovirus) being on the left genomic end, rather than on the right. (Alternatively, this gene may have been captured independently by ancestors of aviadenoviruses and mastadenoviruses.) The dUTPase upregulates the expression of type I interferons, but is not required for viral replication (Deng et al., 2016). The organization of the central part of the genome containing the late genes and the E2 region is similar to that of mastadenoviruses. The right and left ends of the genome contain several transcription units that are unique to aviadenoviruses, and some of the genes in them can be deleted for vector construction, although this may affect replication in cell culture or in vivo in some cases (Pei et al., 2019). The majority of genes and proteins from both ends of the genome have not yet been characterized in detail. GAM-1 (Gallus-anti morte protein, ORF8), located at the right genome end, has been demonstrated to have an anti-apoptotic effect and to activate the heat-shock response in the infected cell. In synergy with another protein encoded by ORF22, it binds the retinoblastoma protein and activates the E2F pathway (Lehrmann and Cotten 1999). Additional and as yet uncharacterized predicted gene products exhibit sequence homology to proteins of other viruses: the non-structural protein NS1 (also known as Rep) of parvoviruses (family Parvoviridae), or the lipase of Marek’s disease virus (family Herpesviridae). Tandem repeats of different length and frequency at the right end of the genome are a common feature of aviadenoviruses. The fiber-1 of both FAdV-1 and FAdV-4 use the coxsackievirus and adenovirus receptor (CAR) for attachment to the cell (Pan et al., 2020). 

Biology

Fowl adenoviruses have been associated with diverse disease patterns, of which inclusion body hepatitis can occur in various bird species (Grgić et al., 2011). In chickens, gizzard erosion is mainly caused by FAdV-1. FAdV-4 is the etiological agent of hepatitis-hydropericardium syndrome mainly in chickens but also in ducks (Schachner et al., 2018). Goose adenovirus 5 seems to have a role in hepatitis and hydropericardium syndrome of goslings (Ivanics et al., 2010). Adenoviruses have been proposed as important pathogens of racing pigeons. They do exist in domestic pigeons but their role has not yet been proven (Ballmann and Harrach 2016, Teske et al., 2017). Aviadenoviruses have been suggested to be pathogenic also in Muscovy duck, parrots and other exotic birds (Zhang et al., 2016, Das et al., 2017). Other aviadenoviruses are infrequently reported in connection with disease in their hosts. FAdV-1 (CELO virus), FAdV-4, FAdV-9 and FAdV-10 have been studied for their feasibility as gene delivery vectors (Corredor et al., 2017). 

Antigenicity

Aviadenoviruses possess no complement-fixing antigen in common with the members of other genera. Regarding serotype specificity, there are isolates that are not easily identifiable by serum neutralization (Schachner et al., 2019). 

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)
• Genome organization (characteristically in the right terminal region)
• Host range
• Pathogenicity
• Cross-neutralization
• Nucleotide composition

For example, the fowl adenovirus serotypes can be grouped into five species on the basis of phylogeny, genome organization and the lack of significant cross-neutralization (Marek et al., 2016, Kaján et al., 2019), and turkey aviadenoviruses have been grouped into three species so far (Marek et al., 2014a). The introduction of types FAdV-8a and FAdV-8b was deemed necessary because of the inconsistency in the type-numbering scheme used in different countries and continents over the years, but this designation does not reflect any closer phylogenetic or serologic relation between the two serotypes. 

Member species

The Member Species table enumerating important virus exemplars classified under each species of the genus is provided at the bottom of the page.

Related, unclassified viruses

Virus names and virus abbreviations are not official ICTV designations. 

Many aviadenoviruses have been detected by consensus PCR (Kaján 2016, Mukai et al., 2019, Verdugo et al., 2019, Jejesky de Oliveira et al., 2020, Rinder et al., 2020, Vaz et al., 2020). Other sequences have been recovered by metagenomics (Vibin et al., 2018, Vibin et al., 2020).