TY - JOUR
T1 - Vertebrate-tropism of a cressdnavirus lineage implicated by poxvirus gene capture
AU - Kinsella, Cormac M.
AU - van der Hoek, Lia
N1 - Funding Information: Computational work was carried out on the Dutch national e-infrastructure with the support of SURF Cooperative. We thank Tim C. Passchier and Jacopo Martelossi for helpful discussions. This work was supported by a grant from the European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie agreement No. 721367, host switching pathogens, infectious outbreaks and zoonosis (HONOURs)), awarded to L.v.d.H. Funding Information: ACKNOWLEDGMENTS. Computational work was carried out on the Dutch national e-infrastructure with the support of SURF Cooperative. We thank Tim C.PasschierandJacopoMartelossiforhelpfuldiscussions.Thisworkwassupported by a grant from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie agreement No. 721367, host switching pathogens, infectious outbreaks and zoonosis (HONOURs)), awarded to L.v.d.H. Publisher Copyright: Copyright © 2023 the Author(s).
PY - 2023/5/16
Y1 - 2023/5/16
N2 - Among cressdnaviruses, only the family Circoviridae is recognized to infect vertebrates, while many others have unknown hosts. Detection of virus-to-host horizontal gene transfer is useful for solving such virus-host relationships. Here, we extend this utility to an unusual case of virus-to-virus horizontal transfer, showing multiple ancient captures of cressdnavirus Rep genes by avipoxviruses-large dsDNA pathogens of birds and other saurians. As gene transfers must have occurred during virus coinfections, saurian hosts were implied for the cressdnavirus donor lineage. Surprisingly, phylogenetic analysis revealed that donors were not members of the vertebrate-infecting Circoviridae, instead belonging to a previously unclassified family that we name Draupnirviridae. While draupnirviruses still circulate today, we show that those in the genus Krikovirus infected saurian vertebrates at least 114 Mya, leaving endogenous viral elements inside snake, lizard, and turtle genomes throughout the Cretaceous Period. Endogenous krikovirus elements in some insect genomes and frequent detection in mosquitoes imply that spillover to vertebrates was arthropod mediated, while ancestral draupnirviruses likely infected protists before their emergence in animals. A modern krikovirus sampled from an avipoxvirus-induced lesion shows that their interaction with poxviruses is ongoing. Captured Rep genes in poxvirus genomes often have inactivated catalytic motifs, yet near-total presence across the Avipoxvirus genus, and evidence of both expression and purifying selection on them suggests currently unknown functions.
AB - Among cressdnaviruses, only the family Circoviridae is recognized to infect vertebrates, while many others have unknown hosts. Detection of virus-to-host horizontal gene transfer is useful for solving such virus-host relationships. Here, we extend this utility to an unusual case of virus-to-virus horizontal transfer, showing multiple ancient captures of cressdnavirus Rep genes by avipoxviruses-large dsDNA pathogens of birds and other saurians. As gene transfers must have occurred during virus coinfections, saurian hosts were implied for the cressdnavirus donor lineage. Surprisingly, phylogenetic analysis revealed that donors were not members of the vertebrate-infecting Circoviridae, instead belonging to a previously unclassified family that we name Draupnirviridae. While draupnirviruses still circulate today, we show that those in the genus Krikovirus infected saurian vertebrates at least 114 Mya, leaving endogenous viral elements inside snake, lizard, and turtle genomes throughout the Cretaceous Period. Endogenous krikovirus elements in some insect genomes and frequent detection in mosquitoes imply that spillover to vertebrates was arthropod mediated, while ancestral draupnirviruses likely infected protists before their emergence in animals. A modern krikovirus sampled from an avipoxvirus-induced lesion shows that their interaction with poxviruses is ongoing. Captured Rep genes in poxvirus genomes often have inactivated catalytic motifs, yet near-total presence across the Avipoxvirus genus, and evidence of both expression and purifying selection on them suggests currently unknown functions.
KW - Avipoxvirus
KW - Draupnirviridae
KW - Krikovirus
KW - horizontal gene transfer
KW - vertebrate host
UR - http://www.scopus.com/inward/record.url?scp=85158158343&partnerID=8YFLogxK
U2 - https://doi.org/10.1073/pnas.2303844120
DO - https://doi.org/10.1073/pnas.2303844120
M3 - Article
C2 - 37155884
SN - 0027-8424
VL - 120
SP - e2303844120
JO - PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
JF - PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
IS - 20
M1 - e2303844120
ER -