Penton blooming, a conserved mechanism of genome delivery used by disparate microviruses

Pavol Bardy*, Conor I.W. MacDonald, Paul C. Kirchberger, Huw T. Jenkins, Tibor Botka, Lewis Byrom, Nawshin T.B. Alim, Daouda A.K. Traore, Hannah C. Koenig, Tristan R. Nicholas, Maria Chechik, Samuel J. Hart, Johan P. Turkenburg, James N. Blaza, J. Thomas Beatty, Paul C.M. Fogg, Alfred A. Antson*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Microviruses are single-stranded DNA viruses infecting bacteria, characterized by T = 1 shells made of single jelly-roll capsid proteins. To understand how microviruses infect their host cells, we have isolated and studied an unusually large microvirus, Ebor. Ebor belongs to the proposed “Tainavirinae” subfamily of Microviridae and infects the model Alphaproteobacterium Rhodobacter capsulatus. Using cryogenic electron microscopy, we show that the enlarged capsid of Ebor is the result of an extended C-terminus of the major capsid protein. The extra packaging space accommodates genes encoding a lytic enzyme and putative methylase, both absent in microviruses with shorter genomes. The capsid is decorated with protrusions at its 3-fold axes, which we show to recognize lipopolysaccharides on the host surface. Cryogenic electron tomography shows that during infection, Ebor attaches to the host cell via five such protrusions. This attachment brings a single pentameric capsomer into close contact with the cell membrane, creating a special vertex through which the genome is ejected. Both subtomogram averaging and single particle analysis identified two intermediates of capsid opening, showing that the interacting penton opens from its center via the separation of individual capsomer subunits. Structural comparison with the model Bullavirinae phage phiX174 suggests that this genome delivery mechanism may be widely present across Microviridae.

Original languageEnglish
Number of pages23
JournalMBio
Volume16
Issue number4
DOIs
Publication statusPublished - 19 Mar 2025

Bibliographical note

© 2025 Bardy et al.

Keywords

  • electron microscopy
  • Microviridae
  • Rhodobacter
  • structural biology
  • virion structure

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