Known and novel parvoviruses identified in domestic pigeons

Abstract

Background: Parvoviridae is a family of single-stranded linear DNA viruses whose members infect both vertebrate and invertebrate species of animals, causing diseases of various systems and often associated with pathology of the gastrointestinal tract. Additionally, parvoviruses are known to induce illnesses causing diarrhea in various avian species as well; however, data on their occurrence and pathology in pigeons is scarce.

Results: In this study, we developed molecular biology methods to detect and quantify parvovirus genetic material in samples acquired from racing pigeons of different health status. Our intention was to determine a connection between the presence of the virus and the occurrence of clinical signs in sampled birds. The results of quantitative analysis indicate no direct association of parvoviruses with the manifestation of enteric disease in pigeons. High-throughput sequencing was performed on samples testing positive in quantitative PCR with TaqMan probe and in digital droplet PCR. It allowed us to assemble two coding-complete pigeon parvovirus genomes, one belonging to new species and referred to as pigeon parvovirus 2, and the second which is a member of species Aveparvovirus columbid1. Additionally, we analyze two coding-complete genomic sequences acquired from pigeon feces in USA, one representing species Aveparvovirus columbid1 and one being a member of Chaphamaparvovirus genus in Hamaparvovirinae subfamily.

Conclusions: This is the first report of parvovirus in pigeons outside Asia. The findings of our research emphasize the need to further explore the poorly understood biology and pathology of pigeon parvoviruses.

Keywords: Columbidae; Parvoviridae; Coding-complete genome; Digital droplet PCR; Enteropathy; High-throughput sequencing; Pigeon; SsDNA virus.

Fig. 1

The graphical presentation of the results of ddPCR in samples testing positive for pigeon parvovirus genetic material in both study and control group, expressed as mean genome copy number per 20 μl of the sample. Blank squares represent the mean values in the two study groups. The difference in genome copy number between the groups was found non-significant in non-parametric Mann–Whitney U test with p = 0.1922

Fig. 2

Schematic illustration of genome organization of coding-complete genome sequences of pigeon parvoviruses obtained in this study: a pigeon parvovirus 1 sequences from USA and Poland, b proposed pigeon parvovirus 2 sequence from Poland, and c pigeon chaphamaparvovirus sequence from USA

Fig. 3

a Maximum likelihood phylogenetic tree made with LG + G substitution model with 1,000 bootstrap replicates, composed of amino acid sequences of NS1 of aveparvoviruses described in this study along with those acquired from GenBank database. The novel sequences described in this study are labeled with accession number and strain name, with pigeon aveparvoviruses from Poland written in bold, while the rest of the sequences is labeled with accession number and host name. The pigeon aveparvoviruses are colored with turquoise and the other aveparvovirus sequences are colored with navy blue. The tree is rooted with a sequence of bovine parvovirus 1 of Bocaparvovirus genus and this sequence is colored with red. b Pairwise identity matrix of amino acid sequences of non-structural protein (NS1) of aveparvoviruses described in this study along with those acquired from GenBank database. All the sequences are labeled with accession number, and accession numbers of pigeon parvoviruses from Poland are written in bold. The amino acid identity of every pair of sequences is represented on a matrix by a color corresponding to the percentage value – from dark blue representing the lowest identity percentage to dark red representing the highest identity percentage. c Maximum likelihood phylogenetic tree made with LG + G + I + F substitution model with 1,000 bootstrap replicates, composed of amino acid sequence of NS1 of pigeon chaphamaparvovirus described in this study along with avian chaphamaparvoviruses acquired from GenBank database. The novel sequence described in this study is labeled with accession number and strain name, while the rest of the sequences is labeled with accession number and host name. The pigeon chaphamaparvoviruses are colored with pink and the other chaphamaparvovirus sequences are colored with purple. The tree is rooted with a sequence of Syngnathus scovelli chapparvovirus of Ichtchaphamaparvovirus genus and this sequence is colored with green. d Pairwise identity matrix of amino acid sequences of non-structural protein (NS1) of pigeon chaphamaparvovirus described in this study along with avian chaphamaparvoviruses acquired from GenBank database. All the sequences are labeled with accession number. The amino acid identity of every pair of sequences is represented on a matrix by a color corresponding to the percentage value – from dark blue representing the lowest identity percentage to dark red representing the highest identity percentage

Fig. 4

Maximum likelihood phylogenetic trees made with GTR + G + I substitution model, composed of pigeon parvovirus sequences described in this study along with other representants of Parvoviridae family acquired from GenBank database: a tree of complete genomic sequences of aveparvoviruses, b tree of VP gene sequences of aveparvoviruses, c tree of complete genomic sequences of avian chaphamaparvoviruses, d tree of VP gene sequences of avian chaphamaparvoviruses. The number of bootstrap replicates is 1,000. Both aveparvovirus trees are rooted with a sequence of bovine parvovirus 1 of Bocaparvovirus genus, while both chaphamaparvovirus trees are rooted with a sequence of Syngnathus scovelli chapparvovirus of Ichtchaphamaparvovirus genus. The sequences described in this study are labeled with accession number and strain name, with pigeon parvoviruses from Poland written in bold, while the rest of the sequences is labeled with accession number and host name. The aveparvovirus sequences are colored with navy blue with the exception of pigeon aveparvoviruses colored with turquoise, and the bocaparvovirus sequence is colored with red. In turn, the chaphamaparvovirus sequences are colored with purple with the exception of pigeon chaphamaparoviruses colored with pink, and the ichtchaphamaparvovirus sequence is colored with green