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Primordial Capsid and Spooled ssDNA Genome Structures Unravel Ancestral Events of Eukaryotic Viruses

Munke, Anna LU orcid ; Kimura, Kei ; Tomaru, Yuji ; Wang, Han ; Yoshiuchi, Kazuhiro ; Mito, Seiya ; Hongo, Yuki and Okamoto, Kenta (2022) In mBio 13(4).
Abstract

Marine algae viruses are important for controlling microorganism communities in the marine ecosystem and played fundamental roles during the early events of viral evolution. Here, we have focused on one major group of marine algae viruses, the single-stranded DNA (ssDNA) viruses from the Bacilladnaviridae family. We present the capsid structure of the bacilladnavirus Chaetoceros tenuissimus DNA virus type II (CtenDNAV-II), determined at 2.4-Å resolution. A structure-based phylogenetic analysis supported the previous theory that bacilladnaviruses have acquired their capsid protein via horizontal gene transfer from a ssRNA virus. The capsid protein contains the widespread virus jelly-roll fold but has additional unique features; a third... (More)

Marine algae viruses are important for controlling microorganism communities in the marine ecosystem and played fundamental roles during the early events of viral evolution. Here, we have focused on one major group of marine algae viruses, the single-stranded DNA (ssDNA) viruses from the Bacilladnaviridae family. We present the capsid structure of the bacilladnavirus Chaetoceros tenuissimus DNA virus type II (CtenDNAV-II), determined at 2.4-Å resolution. A structure-based phylogenetic analysis supported the previous theory that bacilladnaviruses have acquired their capsid protein via horizontal gene transfer from a ssRNA virus. The capsid protein contains the widespread virus jelly-roll fold but has additional unique features; a third b-sheet and a long C-terminal tail. Furthermore, a low-resolution reconstruction of the CtenDNAV-II genome revealed a partially spooled structure, an arrangement previously only described for dsRNA and dsDNA viruses. Together, these results exemplify the importance of genetic recombination for the emergence and evolution of ssDNA viruses and provide important insights into the underlying mechanisms that dictate genome organization. IMPORTANCE Single-stranded DNA (ssDNA) viruses are an extremely widespread group of viruses that infect diverse hosts from all three domains of life, consequently having great economic, medical, and ecological importance. In particular, bacilladnaviruses are highly abundant in marine sediments and greatly influence the dynamic appearance and disappearance of certain algae species. Despite the importance of ssDNA viruses and the last couple of years’ advancements in cryo-electron microscopy, structural information on the genomes of ssDNA viruses remains limited. This paper describes two important achievements: (i) the first atomic structure of a bacilladnavirus capsid, which revealed that the capsid protein gene presumably was acquired from a ssRNA virus in early evolutionary events; and (ii) the structural organization of a ssDNA genome, which retains a spooled arrangement that previously only been observed for double-stranded viruses.

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author
; ; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
subject
keywords
bacilladnavirus, capsid protein evolution, diatom virus, genome structure, horizontal gene transfer, algal virus, nodavirus, ssDNA virus, virus, capsid structure, cryo-EM, cryo-electron microscopy, Virus, kiselalgsvirus, kryo-EM
in
mBio
volume
13
issue
4
article number
e00156-22
publisher
American Society for Microbiology
external identifiers
  • scopus:85137126091
  • pmid:35856561
ISSN
2161-2129
DOI
10.1128/mbio.00156-22
language
English
LU publication?
no
additional info
Publisher Copyright: Copyright © 2022 Munke et al.
id
64781ca1-0871-497e-8898-75515559daf6
date added to LUP
2025-04-18 21:22:00
date last changed
2025-07-12 04:36:55
@article{64781ca1-0871-497e-8898-75515559daf6,
  abstract     = {{<p>Marine algae viruses are important for controlling microorganism communities in the marine ecosystem and played fundamental roles during the early events of viral evolution. Here, we have focused on one major group of marine algae viruses, the single-stranded DNA (ssDNA) viruses from the Bacilladnaviridae family. We present the capsid structure of the bacilladnavirus Chaetoceros tenuissimus DNA virus type II (CtenDNAV-II), determined at 2.4-Å resolution. A structure-based phylogenetic analysis supported the previous theory that bacilladnaviruses have acquired their capsid protein via horizontal gene transfer from a ssRNA virus. The capsid protein contains the widespread virus jelly-roll fold but has additional unique features; a third b-sheet and a long C-terminal tail. Furthermore, a low-resolution reconstruction of the CtenDNAV-II genome revealed a partially spooled structure, an arrangement previously only described for dsRNA and dsDNA viruses. Together, these results exemplify the importance of genetic recombination for the emergence and evolution of ssDNA viruses and provide important insights into the underlying mechanisms that dictate genome organization. IMPORTANCE Single-stranded DNA (ssDNA) viruses are an extremely widespread group of viruses that infect diverse hosts from all three domains of life, consequently having great economic, medical, and ecological importance. In particular, bacilladnaviruses are highly abundant in marine sediments and greatly influence the dynamic appearance and disappearance of certain algae species. Despite the importance of ssDNA viruses and the last couple of years’ advancements in cryo-electron microscopy, structural information on the genomes of ssDNA viruses remains limited. This paper describes two important achievements: (i) the first atomic structure of a bacilladnavirus capsid, which revealed that the capsid protein gene presumably was acquired from a ssRNA virus in early evolutionary events; and (ii) the structural organization of a ssDNA genome, which retains a spooled arrangement that previously only been observed for double-stranded viruses.</p>}},
  author       = {{Munke, Anna and Kimura, Kei and Tomaru, Yuji and Wang, Han and Yoshiuchi, Kazuhiro and Mito, Seiya and Hongo, Yuki and Okamoto, Kenta}},
  issn         = {{2161-2129}},
  keywords     = {{bacilladnavirus; capsid protein evolution; diatom virus; genome structure; horizontal gene transfer; algal virus; nodavirus; ssDNA virus; virus; capsid structure; cryo-EM; cryo-electron microscopy; Virus; kiselalgsvirus; kryo-EM}},
  language     = {{eng}},
  number       = {{4}},
  publisher    = {{American Society for Microbiology}},
  series       = {{mBio}},
  title        = {{Primordial Capsid and Spooled ssDNA Genome Structures Unravel Ancestral Events of Eukaryotic Viruses}},
  url          = {{http://dx.doi.org/10.1128/mbio.00156-22}},
  doi          = {{10.1128/mbio.00156-22}},
  volume       = {{13}},
  year         = {{2022}},
}