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. 2010 Apr;84(8):3889-97.
doi: 10.1128/JVI.02497-09. Epub 2010 Jan 20.

Host range, prevalence, and genetic diversity of adenoviruses in bats

Yan Li  1 , Xingyi Ge, Huajun Zhang, Peng Zhou, Yan Zhu, Yunzhi Zhang, Junfa Yuan, Lin-Fa Wang, Zhengli Shi
Affiliations

Host range, prevalence, and genetic diversity of adenoviruses in bats

Yan Li et al. J Virol. 2010 Apr.

Abstract

Bats are the second largest group of mammals on earth and act as reservoirs of many emerging viruses. In this study, a novel bat adenovirus (AdV) (BtAdV-TJM) was isolated from bat fecal samples by using a bat primary kidney cell line. Infection studies indicated that most animal and human cell lines are susceptible to BtAdV-TJM, suggesting a possible wide host range. Genome analysis revealed 30 putative genes encoding proteins homologous to their counterparts in most known AdVs. Phylogenetic analysis placed BtAdV-TJM within the genus Mastadenovirus, most closely related to tree shrew and canine AdVs. PCR analysis of 350 bat fecal samples, collected from 19 species in five Chinese provinces during 2007 and 2008, indicated that 28 (or 8%) samples were positive for AdVs. The samples were from five bat species, Hipposideros armiger, Myotis horsfieldii, M. ricketti, Myotis spp., and Scotophilus kuhlii. The prevalence ranged from 6.25% (H. armiger in 2007) to 40% (M. ricketti in 2007). Comparison studies based on available partial sequences of the pol gene demonstrated a great genetic diversity among bat AdVs infecting different bat species as well as those infecting the same bat species. This is the first report of a genetically diverse group of DNA viruses in bats. Our results support the notion, derived from previous studies based on RNA viruses (especially coronaviruses and astroviruses), that bats seem to have the unusual ability to harbor a large number of genetically diverse viruses within a geographic location and/or within a taxonomic group.

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Figures

FIG. 1.
FIG. 1.
Isolation of bat adenovirus in bat primary kidney cells. (A) Noninfected bat primary kidney cells. (B) The same cells as those shown in A after infection with BtAdV-TJM at 2 PFU/cell, showing CPEs observed at 24 h postinfection.
FIG. 2.
FIG. 2.
Examination of viral particles by electron microscopy. See Materials and Methods for a description of the preparation of the samples.
FIG. 3.
FIG. 3.
Genome organization of BtAdV-TJM. The viral genome is represented by the double line in the center marked with 5-kbp intervals. Protein-coding regions are shown as filled arrows. Arrows above the black line represent open reading frames (ORFs) encoded on the forward (top) strand oriented from left to right. Arrows underneath the genome line represent ORFs that are carried on the complementary (bottom) strand. ORFs were named according to the nomenclature used for homologous proteins of other AdVs.
FIG. 4.
FIG. 4.
Phylogenetic analysis of bat adenoviruses. The phylogenetic trees were constructed based on the alignment of full-length AdV genome nucleotide sequences (A), the amino acid sequences of hexon proteins (B), and partial amino acid sequences of the polymerases (C) of bat adenoviruses by using the neighbor-joining (NJ) method with a bootstrap of 1,000 replicates with the MEGA 4.1 program. Gaps were regarded as a complete deletion unless otherwise specified. A condensed tree is presented in C. The scale bar is in units of nucleotide (A) or amino acid (B and C) residue substitutions per site. Bootstrap values (percent) are indicated at the branch nodes of the phylogenetic trees. Abbreviations are as follows (with GenBank accession numbers in parentheses): HAdV-A, human adenovirus A (accession no. NC_001460); HAdV-B1, human adenovirus B1 (accession no. NC_011203); HAdV-B2, human adenovirus B2 (accession no. NC_011202); HAdV-C, Human adenovirus C (NC_001405); HAdV-D, human adenovirus D (accession no. NC_010956); HAdV-E, human adenovirus E (accession no. NC_003266); HAdV-F, human adenovirus F (accession no. NC_001454); OAdV-A, ovine adenovirus A (accession no. NC_002513); OAdV-D, ovine adenovirus D (accession no. NC_004037); PoAdV-C, porcine adenovirus C (accession no. NC_002702); BAdV-B, bovine adenovirus B (accession no. NC_001876); BAdV-D, bovine adenovirus D (accession no. NC_002685); CAdV-1, canine adenovirus 1 (accession no. NC_001734); CAdV-2, canine adenovirus 2 (accession no. AC_000020); MAdV-A, murine adeno- virus A (accession no. NC_000942); TsAdV, tree shrew adenovirus (accession no. NC_004453); SnAdV, snake adenovirus (accession no. NC_009989); FrAdV, frog adenovirus (accession no. NC_002501); TAdV-A, turkey adenovirus A (accession no. NC_001958); FAdV-A, fowl adenovirus A (accession no. NC_001720); FAdV-D, fowl adenovirus D (accession no. NC_000899); DAdV-A, duck adenovirus A (accession no. NC_001813); bat AdV-FBV1, bat adenovirus FBV1 (accession no. AB303301). The bat AdV detected in this study is named by the sample number followed by the abbreviation of the sampling location and species name. The sequences derived from different locations are highlighted with different symbols. HB, Hubei; HN, Hainan; GD, Guangdong; YN, Yunnan; TJ, Tianjin; Ha, Hipposideros armiger; Md, Myotis daubentoni; Mh, Myotis horsfieldii; Mspp, unidentified Myotis species; Mr, Myotis ricketti; SK, Scotophilus kuhlii.
FIG. 4.
FIG. 4.
Phylogenetic analysis of bat adenoviruses. The phylogenetic trees were constructed based on the alignment of full-length AdV genome nucleotide sequences (A), the amino acid sequences of hexon proteins (B), and partial amino acid sequences of the polymerases (C) of bat adenoviruses by using the neighbor-joining (NJ) method with a bootstrap of 1,000 replicates with the MEGA 4.1 program. Gaps were regarded as a complete deletion unless otherwise specified. A condensed tree is presented in C. The scale bar is in units of nucleotide (A) or amino acid (B and C) residue substitutions per site. Bootstrap values (percent) are indicated at the branch nodes of the phylogenetic trees. Abbreviations are as follows (with GenBank accession numbers in parentheses): HAdV-A, human adenovirus A (accession no. NC_001460); HAdV-B1, human adenovirus B1 (accession no. NC_011203); HAdV-B2, human adenovirus B2 (accession no. NC_011202); HAdV-C, Human adenovirus C (NC_001405); HAdV-D, human adenovirus D (accession no. NC_010956); HAdV-E, human adenovirus E (accession no. NC_003266); HAdV-F, human adenovirus F (accession no. NC_001454); OAdV-A, ovine adenovirus A (accession no. NC_002513); OAdV-D, ovine adenovirus D (accession no. NC_004037); PoAdV-C, porcine adenovirus C (accession no. NC_002702); BAdV-B, bovine adenovirus B (accession no. NC_001876); BAdV-D, bovine adenovirus D (accession no. NC_002685); CAdV-1, canine adenovirus 1 (accession no. NC_001734); CAdV-2, canine adenovirus 2 (accession no. AC_000020); MAdV-A, murine adeno- virus A (accession no. NC_000942); TsAdV, tree shrew adenovirus (accession no. NC_004453); SnAdV, snake adenovirus (accession no. NC_009989); FrAdV, frog adenovirus (accession no. NC_002501); TAdV-A, turkey adenovirus A (accession no. NC_001958); FAdV-A, fowl adenovirus A (accession no. NC_001720); FAdV-D, fowl adenovirus D (accession no. NC_000899); DAdV-A, duck adenovirus A (accession no. NC_001813); bat AdV-FBV1, bat adenovirus FBV1 (accession no. AB303301). The bat AdV detected in this study is named by the sample number followed by the abbreviation of the sampling location and species name. The sequences derived from different locations are highlighted with different symbols. HB, Hubei; HN, Hainan; GD, Guangdong; YN, Yunnan; TJ, Tianjin; Ha, Hipposideros armiger; Md, Myotis daubentoni; Mh, Myotis horsfieldii; Mspp, unidentified Myotis species; Mr, Myotis ricketti; SK, Scotophilus kuhlii.
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