Opportunistic sampling of wild native and invasive birds reveals a rich diversity of adenoviruses in Australia

Abstract

Little is known about the diversity of adenoviruses in wild birds and how they have evolved and are maintained in complex ecosystems. In this study, 409 samples were collected from woodland birds caught for banding (droppings), birds submitted to a wildlife hospital (droppings and tissues), silver gulls (droppings or tissues), and feral pigeons (Columbia livia; oral, cloacal swabs, or tissues) from the Greater Sydney area in NSW, Australia. Additional samples were from native pigeons and doves (swabs) presented to the Healesville Sanctuary, VIC, Australia. Samples were screened for adenovirus DNA using degenerate primers and polymerase chain reaction. Adenovirus sequences were detected in eighty-three samples representing thirty-five novel amino acid sequences. Fourteen novel sequences were atadenoviruses, seven were aviadenoviruses, twelve were siadenoviruses, and one was a mastadenovirus. Sequences from passerine birds were predominately found to form a single lineage within the atadenoviruses, a second lineage in the siadenoviruses, and a third smaller aviadenovirus lineage. These viruses appeared to have co-evolved with a diverse group of woodland birds that share similar habitat. Evidence for host/virus co-evolution in some viruses and a wide host range in others was observed. A high prevalence of adenovirus infection was found in rainbow lorikeets (Trichoglossus haematodus), galahs (Eolophus roseicapilla), and sulphur-crested cockatoos (Cacatua galerita). Sequences were either identical to or mapped to already established lineages in the Aviadenovirus, Siadenovirus, and Atadenovirus genera, suggesting a possible origin of the psittacine adenoviruses in ancestral Australian psittacine birds. The sequences of passerine and psittacine origin provided insight into diversity and structure of the Atadenovirus genus and demonstrated for the first-time viruses of passerine origin in the Aviadenovirus genus. Four unrelated adenovirus sequences were found in silver gull samples (Chroicocephalus novaehollandiae), including one of pigeon origin, suggesting environmental virus exposure. Three pigeon adenovirus types were detected in feral pigeons and infection prevalence was high. Evidence for host switching between invasive species and native species and native species and invasive species was documented. A variant of a murine adenovirus was detected in kidney tissue from two bird species suggesting mouse to bird transmission.

Molecular Characterisation of a Novel and Highly Divergent Passerine Adenovirus 1

“…Similar to the balanced G+C contents in reptilian atadenoviruses and PsAdV-3 genome sequence [ 5 , 10 , 11 ], the novel PaAdV-1 genome sequence also showed a balanced G+C content (53.70), in contrast to the G+C content seen with most of the of avian and ruminant atadenoviruses ( Table 2 ). Interestingly, a very recent study has shown that the greatest diversity existed in the G+C contents in partial DNA polymerase gene of atadenoviruses that was originally sequenced from similar species of birds [ 4 ]. This scenario highlights that the low G+C content is not likely a consistent feature of the genus Atadenovirus , and it would be reasonable to take careful consideration to distinguish relatively closely related viruses based on G+C contents.…”

“…The total genomic DNA was extracted from collected droppings, using a commercial kit (PurelinkTM Genomic DNA Mini Kit, Invitrogen, California, CA, USA) according to the manufacturer’s instructions. Initially, the extracted DNA was screened for the presence of adenoviruses, using an established PCR protocol that has been widely used to detect adenoviruses, and, based on a short amino acid sequence of the DNA polymerase gene, it was found to be an atadenovirus whose sequence clustered with atadenoviruses derived from other Australian passerine species [ 4 ].…”

“…One of these genera, the Atadenovirus , was added in 2002, to include adenoviruses that were previously assigned to the genus Mastadenovirus , but varied significantly based on genomic size, structure, genes, and gene arrangement. Originally all the viruses in the genus were thought to have an A+T content bias [ 2 , 3 ], but with the discovery of new species in this genus, it has been shown that the A+T bias is not a consistent feature of this genus [ 4 , 5 , 6 ]. The size of sequenced atadenovirus genomes ranges between 27 and 34 kb, and all have the characteristic inverted terminal repeat (ITR) found in all adenoviruses [ 7 ].…”

“…Atadenoviruses have been detected in a diverse range of hosts, including birds [ 4 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 ], reptiles (order Squamata; lizards, snakes, and worm lizards), ruminants [ 8 , 9 , 15 , 19 ], marsupials [ 20 , 21 ], and a common tortoise [ 22 ]. Using a partial DNA polymerase gene sequence, recent studies also report the presence of a large number of novel atadenoviruses circulating in wild passerine species of birds in Australia and Europe and passerine species kept in aviculture collections [ 4 , 17 , 18 ]. Because of the limited sequence information for these passerine adenoviruses, there is still considerable uncertainty about their phylogenetic relationship to each other and other atadenoviruses.…”

Isolation and molecular characterization of Fowl adenovirus strains in Black grouse: First reported case in Poland

“…Novel DNA sequences identified from four of the adenovirus genera (Aviadenovirus, Atadenovirus, Siadenovirus, and Mastadenovirus) have important implications for our understanding of adenovirus history and evolution [33].…”