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@ARTICLE{Lauber:289663,
author = {C. Lauber and X. Zhang and J. Vaas$^*$ and F. Klingler$^*$
and P. Mutz$^*$ and A. Dubin and T. Pietschmann and O. Roth
and B. W. Neuman and A. E. Gorbalenya and R.
Bartenschlager$^*$ and S. Seitz$^*$},
title = {{D}eep mining of the {S}equence {R}ead {A}rchive reveals
major genetic innovations in coronaviruses and other
nidoviruses of aquatic vertebrates.},
journal = {PLoS pathogens},
volume = {20},
number = {4},
issn = {1553-7366},
address = {Lawrence, Kan.},
publisher = {PLoS},
reportid = {DKFZ-2024-00845},
pages = {e1012163 -},
year = {2024},
note = {#LA:F170#LA:D430#},
abstract = {Virus discovery by genomics and metagenomics empowered
studies of viromes, facilitated characterization of pathogen
epidemiology, and redefined our understanding of the natural
genetic diversity of viruses with profound functional and
structural implications. Here we employed a data-driven
virus discovery approach that directly queries unprocessed
sequencing data in a highly parallelized way and involves a
targeted viral genome assembly strategy in a wide range of
sequence similarity. By screening more than 269,000 datasets
of numerous authors from the Sequence Read Archive and using
two metrics that quantitatively assess assembly quality, we
discovered 40 nidoviruses from six virus families whose
members infect vertebrate hosts. They form 13 and 32
putative viral subfamilies and genera, respectively, and
include 11 coronaviruses with bisegmented genomes from
fishes and amphibians, a giant 36.1 kilobase coronavirus
genome with a duplicated spike glycoprotein (S) gene, 11
tobaniviruses and 17 additional corona-, arteri-, cremega-,
nanhypo- and nangoshaviruses. Genome segmentation emerged in
a single evolutionary event in the monophyletic lineage
encompassing the subfamily Pitovirinae. We recovered the
bisegmented genome sequences of two coronaviruses from RNA
samples of 69 infected fishes and validated the presence of
poly(A) tails at both segments using 3'RACE PCR and
subsequent Sanger sequencing. We report a genetic linkage
between accessory and structural proteins whose phylogenetic
relationships and evolutionary distances are incongruent
with the phylogeny of replicase proteins. We rationalize
these observations in a model of inter-family S
recombination involving at least five ancestral corona- and
tobaniviruses of aquatic hosts. In support of this model, we
describe an individual fish co-infected with members from
the families Coronaviridae and Tobaniviridae. Our results
expand the scale of the known extraordinary evolutionary
plasticity in nidoviral genome architecture and call for
revisiting fundamentals of genome expression, virus particle
biology, host range and ecology of vertebrate nidoviruses.},
cin = {F170 / D430},
ddc = {610},
cid = {I:(DE-He78)F170-20160331 / I:(DE-He78)D430-20160331},
pnm = {314 - Immunologie und Krebs (POF4-314)},
pid = {G:(DE-HGF)POF4-314},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:38648214},
doi = {10.1371/journal.ppat.1012163},
url = {https://inrepo02.dkfz.de/record/289663},
}