Dataset Information

Mammalian deltavirus without hepadnavirus coinfection in the neotropical rodent Proechimys semispinosus.

ABSTRACT: Hepatitis delta virus (HDV) is a human hepatitis-causing RNA virus, unrelated to any other taxonomic group of RNA viruses. Its occurrence as a satellite virus of hepatitis B virus (HBV) is a singular case in animal virology for which no consensus evolutionary explanation exists. Here we present a mammalian deltavirus that does not occur in humans, identified in the neotropical rodent species Proechimys semispinosus The rodent deltavirus is highly distinct, showing a common ancestor with a recently described deltavirus in snakes. Reverse genetics based on a tandem minus-strand complementary DNA genome copy under the control of a cytomegalovirus (CMV) promoter confirms autonomous genome replication in transfected cells, with initiation of replication from the upstream genome copy. In contrast to HDV, a large delta antigen is not expressed and the farnesylation motif critical for HBV interaction is absent from a genome region that might correspond to a hypothetical rodent large delta antigen. Correspondingly, there is no evidence for coinfection with an HBV-related hepadnavirus based on virus detection and serology in any deltavirus-positive animal. No other coinfecting viruses were detected by RNA sequencing studies of 120 wild-caught animals that could serve as a potential helper virus. The presence of virus in blood and pronounced detection in reproductively active males suggest horizontal transmission linked to competitive behavior. Our study establishes a nonhuman, mammalian deltavirus that occurs as a horizontally transmitted infection, is potentially cleared by immune response, is not focused in the liver, and possibly does not require helper virus coinfection.

SUBMITTER: Paraskevopoulou S

PROVIDER: S-EPMC7395443 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Mammalian deltavirus without hepadnavirus coinfection in the neotropical rodent <i>Proechimys semispinosus</i>.

Paraskevopoulou Sofia S Pirzer Fabian F Goldmann Nora N Schmid Julian J Corman Victor Max VM Gottula Lina Theresa LT Schroeder Simon S Rasche Andrea A Muth Doreen D Drexler Jan Felix JF Heni Alexander Christoph AC Eibner Georg Joachim GJ Page Rachel A RA Jones Terry C TC Müller Marcel A MA Sommer Simone S Glebe Dieter D Drosten Christian C

Proceedings of the National Academy of Sciences of the United States of America 20200710 30

Hepatitis delta virus (HDV) is a human hepatitis-causing RNA virus, unrelated to any other taxonomic group of RNA viruses. Its occurrence as a satellite virus of hepatitis B virus (HBV) is a singular case in animal virology for which no consensus evolutionary explanation exists. Here we present a mammalian deltavirus that does not occur in humans, identified in the neotropical rodent species <i>Proechimys semispinosus</i> The rodent deltavirus is highly distinct, showing a common ancestor with a ...[more]

PMID: 32651267

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Project description:Hepatitis D virus (HDV) forms the genus Deltavirus unassigned to any virus family. HDV is a satellite virus and needs hepatitis B virus (HBV) to make infectious particles. Deltaviruses are thought to have evolved in humans, since for a long time, they had not been identified elsewhere. Herein we report, prompted by the recent discovery of an HDV-like agent in birds, the identification of a deltavirus in snakes (Boa constrictor) designated snake HDV (sHDV). The circular 1,711-nt RNA genome of sHDV resembles human HDV (hHDV) in its coding strategy and size. We discovered sHDV during a metatranscriptomic study of brain samples of a Boa constrictor breeding pair with central nervous system signs. Applying next-generation sequencing (NGS) to brain, blood, and liver samples from both snakes, we did not find reads matching hepadnaviruses. Sequence comparison showed the snake delta antigen (sHDAg) to be 55% and 37% identical to its human and avian counterparts. Antiserum raised against recombinant sHDAg was used in immunohistology and demonstrated a broad viral target cell spectrum, including neurons, epithelial cells, and leukocytes. Using RT-PCR, we also detected sHDV RNA in two juvenile offspring and in a water python (Liasis macklotisavuensis) in the same snake colony, potentially indicating vertical and horizontal transmission. Screening of 20 randomly selected boas from another breeder by RT-PCR revealed sHDV infection in three additional snakes. The observed broad tissue tropism and the failure to detect accompanying hepadnavirus suggest that sHDV could be a satellite virus of a currently unknown enveloped virus.IMPORTANCE So far, the only known example of deltaviruses is the hepatitis delta virus (HDV). HDV is speculated to have evolved in humans, since deltaviruses were until very recently found only in humans. Using a metatranscriptomic sequencing approach, we found a circular RNA, which resembles that of HDV in size and coding strategy, in a snake. The identification of similar deltaviruses in distantly related species other than humans indicates that the previously suggested hypotheses on the origins of deltaviruses need to be updated. It is still possible that the ancestor of deltaviruses emerged from cellular RNAs; however, it likely would have happened much earlier in evolution than previously thought. These findings open up completely new avenues in evolution and pathogenesis studies of deltaviruses.

Project description:Tuco-tucos (Ctenomys spp.) are subterranean rodents that produce territorial, high intensity long-range vocalizations (LRVs) of broadband and low frequency that are essential for long-distance communication between individuals in different tunnel systems. Despite their importance, the development of LRVs remains poorly understood. In adult Anillaco Tuco-Tucos (Ctenomys sp.) the LRV is composed by two types of syllables (series and individual notes) that are repeated a variable number of times. We studied the development of the LRVs in eight juveniles of the Anillaco Tuco-Tuco ranging from 14-28 to 104-118 days after birth. We (1) tested whether the syllables followed any of three alternative developmental modes (retention of juvenile vocalizations, modification of juvenile precursors or de novo appearance in adults), (2) evaluated the development of structural and acoustic features of syllables, and (3) tested the prediction that juveniles should produce a greater proportion of atypical series in precursors of the LRV than adults, due to lack maturation and/or precise coupling of neuromuscular and anatomical structures. The LRV of the Anillaco Tuco-Tuco exhibited a mixed developmental mode: while series developed from juvenile precursors whose acoustic features gradually approached those of adults, individual notes appeared later in the ontogeny and de novo with acoustic features indistinguishable from those of adults. The number of series per vocalization increased through development and varied from one to 25 in juvenile males and from one to six in juvenile females. The structure of the most common series type (triad) did not exhibit ontogenetic changes and was present as such at the onset of the emission of vocalizations. On the contrary, acoustic features of juvenile triad notes changed with age in both sexes (duration 90% increased through development, while bandwidth 90% and peak frequency decreased). Furthermore, juveniles emitted a higher proportion of atypical series than adults (7.4% vs. 0.3%), as expected in the development of any complex behavior that requires practice to be mastered. The maturation of the LRV occurred well before the sexual maturation, presumably due to the protracted time needed to acquire or build a burrow system long before mating is possible. We propose that protracted vocal development is another component in the slow developmental strategy of Ctenomys and subterranean rodents in general.

Dataset Information

Mammalian deltavirus without hepadnavirus coinfection in the neotropical rodent Proechimys semispinosus.

Publications

Mammalian deltavirus without hepadnavirus coinfection in the neotropical rodent <i>Proechimys semispinosus</i>.

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