Article

Genomic Fossils Calibrate the Long-Term Evolution of Hepadnaviruses

Department of Biology, University of Texas, Arlington, Texas, United States of America.
PLoS Biology (Impact Factor: 9.34). 09/2010; 8(9). DOI: 10.1371/journal.pbio.1000495
Source: PubMed

ABSTRACT

Because most extant viruses mutate rapidly and lack a true fossil record, their deep evolution and long-term substitution rates remain poorly understood. In addition to retroviruses, which rely on chromosomal integration for their replication, many other viruses replicate in the nucleus of their host's cells and are therefore prone to endogenization, a process that involves integration of viral DNA into the host's germline genome followed by long-term vertical inheritance. Such endogenous viruses are highly valuable as they provide a molecular fossil record of past viral invasions, which may be used to decipher the origins and long-term evolutionary characteristics of modern pathogenic viruses. Hepadnaviruses (Hepadnaviridae) are a family of small, partially double-stranded DNA viruses that include hepatitis B viruses. Here we report the discovery of endogenous hepadnaviruses in the genome of the zebra finch. We used a combination of cross-species analysis of orthologous insertions, molecular dating, and phylogenetic analyses to demonstrate that hepadnaviruses infiltrated repeatedly the germline genome of passerine birds. We provide evidence that some of the avian hepadnavirus integration events are at least 19 My old, which reveals a much deeper ancestry of Hepadnaviridae than could be inferred based on the coalescence times of modern hepadnaviruses. Furthermore, the remarkable sequence similarity between endogenous and extant avian hepadnaviruses (up to 75% identity) suggests that long-term substitution rates for these viruses are on the order of 10(-8) substitutions per site per year, which is a 1,000-fold slower than short-term rates estimated based on the sequences of circulating hepadnaviruses. Together, these results imply a drastic shift in our understanding of the time scale of hepadnavirus evolution, and suggest that the rapid evolutionary dynamics characterizing modern avian hepadnaviruses do not reflect their mode of evolution on a deep time scale.

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    • "Subsequent to this landmark study, similar avihepadnaviral elements have been identified in the genome of budgerigars of the order Psittaciformes (Cui and Holmes 2012). Comparative phylogenetic analysis on these endogenous and existing exogenous avian hepadnaviruses established the eZHBVs are far more divergent than modern-day DHBVs and form their own distinct lineages (Gilbert and Feschotte 2010 ), indicative of multiple or recurrent genomic integration events. A more recent study reported a genomic record of Hepadnaviridae endogenizations estimated to have occurred during a period of bird evolution from 12 to 82 mya (Suh et al. 2013), and constituted the first discovery of a Mesozoic paleovirus genome (.82 mya). "
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    ABSTRACT: Members of the family Hepadnaviridae fall into two subgroups: mammalian and avian. The detection of endogenous avian hepadnavirus DNA integrated into the genomes of zebra finches has revealed a deep evolutionary origin of hepadnaviruses that was not previously recognized, dating back at least 40 million and possibly >80 million years ago. The nonprimate mammalian members of the Hepadnaviridae include the woodchuck hepatitis virus (WHV), the ground squirrel hepatitis virus, and arctic squirrel hepatitis virus, as well as a number of members of the recently described bat hepatitis virus. The identification of hepatitis B viruses (HBVs) in higher primates, such as chimpanzee, gorilla, orangutan, and gibbons that cluster with the human HBV, aswell as a number of recombinant forms between humans and primates, further implies a more complex origin of this virus. We discuss the current theories of the origin and evolution of HBVand propose a model that includes crossspecies transmissions and subsequent recombination events on a genetic backbone of genotype C HBV infection. The hepatitis delta virus (HDV) is a defective RNAvirus requiring the presence of the HBV for the completion of its life cycle. The origins of this virus remain unknown, although some recent studies have suggested an ancient African radiation. The age of the association between HDV and HBV is also unknown.
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    • "Hepadnaviridae has had a long existence (>200 million years) in 61 different species (Gilbert and Feschotte, 2010; Katzourakis and 62 Gifford, 2010; Suh et al., 2013). The genomic organization of differ- 63 ent HBV lineages has been conserved over a long time, except for 64 gene X which exists only in mammalian HBVs (Locarnini et al., 65 2013). "

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    • "Many recent reports of statistical analyses of the gene sequences of viruses collected on different dates conclude that extant viruses have large mutation rates and must therefore have originated in the past few hundred or thousand years, but doubts about these interpretations (Firth et al. 2010; Sharp and Simmonds 2011; Duchêne, Holmes, and Ho 2014), and clues of much more ancient origins of some viruses, are forcing a re-think. Much of the doubt has arisen from evidence of viruses or virogenes integrated in the genomes of plants (Bejarano et al. 1996; Geering et al. 2005; Chiba et al. 2011; James et al. 2011; Lefeuvre et al. 2011; Lyttle, Orlovich, and Guy 2011; Kondo et al. 2013; Filloux et al. 2015) and animals (Gifford et al. 2008; Katzourakis et al. 2009; Belyi, Levine, and Skalka 2010a, b; Gilbert and Feschotte 2010; Horie et al. 2010; Taylor et al. 2010, 2011; Worobey et al. 2010; Han and Worobey 2012), where the taxonomy of the integrated genes and their 'hosts' indicates an ancient origin. Attempts to establish ancient origins by phylogenetic evidence of co-divergence of host and virus (e.g. "

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