Genus: Aviadenovirus

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 (Figure 2.Adenoviridae) (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 2Adenoviridae) (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

Exemplar isolate of the species
SpeciesVirus nameIsolateAccession numberRefSeq numberAvailable sequenceVirus Abbrev.
Aviadenovirus leucophthalmiSouthern Psittacara leucophthalmus aviadenovirus (white-eyed parakeet adenovirus 2)MN153802Complete coding genomeWPAdV-2
Duck aviadenovirus Bduck adenovirus 2GRKJ469653NC_024486Complete genomeDAdV-2
Duck aviadenovirus Bduck adenovirus 3FJGT01MH777395Complete genomeDAdV-3
Falcon aviadenovirus Afalcon adenovirus 1DQ460220NC_043092Partial genomeFaAdV-1
Fowl aviadenovirus Afowl adenovirus 1CELO PhelpsU46933AC_000014Complete genomeFAdV-1
Fowl aviadenovirus Bfowl adenovirus 5340KC493646NC_021221Complete genomeFAdV-5
Fowl aviadenovirus Cfowl adenovirus 4KR5HE608152Complete genomeFAdV-4
Fowl aviadenovirus Cfowl adenovirus 10C2-BMK572851Complete genomeFAdV-10
Fowl aviadenovirus Dfowl adenovirus 9A-2AAF083975NC_000899Complete genomeFAdV-9
Fowl aviadenovirus Dfowl adenovirus 2SR48KT862806Complete genomeFAdV-2
Fowl aviadenovirus Dfowl adenovirus 3SR49KT862807Complete genomeFAdV-3
Fowl aviadenovirus Dfowl adenovirus 11380KT862812Complete genomeFAdV-11
Fowl aviadenovirus Efowl adenovirus 6CR119KT862808NC_038332Complete genomeFAdV-6
Fowl aviadenovirus Efowl adenovirus 7YR36KT862809Complete genomeFAdV-7
Fowl aviadenovirus Efowl adenovirus 8aTR59KT862810Complete genomeFAdV-8a
Fowl aviadenovirus Efowl adenovirus 8b764KT862811Complete genomeFAdV-8b
Goose aviadenovirus Agoose adenovirus 4P29JF510462NC_017979Complete genomeGoAdV-4
Pigeon aviadenovirus Apigeon adenovirus 1IDA4FN824512NC_024474Complete genomePiAdV-1
Pigeon aviadenovirus Bpigeon adenovirus 2YPDS-Y-V1.A19.11-2013KX121164NC_031503Complete genomePiAdV-2
Psittacine aviadenovirus Bpsittacine adenovirus 4CS15-4016KX577802NC_039032Complete genomePsAdV-4
Psittacine aviadenovirus Cpsittacine adenovirus 118VIR149_ITA_2018MH580295Complete genomePsAdV-1
Turkey aviadenovirus Bturkey adenovirus 1D90/2GU936707NC_014564Complete genomeTAdV-1
Turkey aviadenovirus Cturkey adenovirus 4TNI1KF477312NC_022612Complete genomeTAdV-4
Turkey aviadenovirus Dturkey adenovirus 51277BTKF477313NC_022613Complete genomeTAdV-5

Virus names, the choice of exemplar isolates and virus abbreviations are not official ICTV designations.

Related, unclassified viruses

Virus name

Accession number

Virus abbreviation

crane adenovirus 1

LC469780

 

duck adenovirus 4

MN733730

DAdV-4

goldfinch adenovirus

MN380553

 

European greenfinch adenovirus strain 48164-T3

MN380554

 

great tit adenovirus strain 47292

MN380547

 

gull adenovirus

KC309438

 

marten-associated adenovirus 1

KY705358

 

Meyer’s parrot adenovirus 1

AY644731

 

neotropic cormorant adenovirus

KY769942

 

Pacific black duck adenovirus

MT894382

 

pigeon adenovirus 3

KX555530

PiAdV-3

smooth billed ani adenovirus 1

MN540448

 

tropical screech owl adenovirus 2

LC536616

 

turkey adenovirus 2

GU936708

TAdV-2

vitelline masked weaver adenovirus strain 39658

MN380540

 

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).