Structural studies demonstrating a bacteriophage-like replication cycle of the eukaryote-infecting Paramecium bursaria chlorella virus-1

Authors

Elad Milrot, The Weizmann Institute of Science, Rehovot, IsraelFollow
Eyal Shimoni, The Weizmann Institute of Science, Rehovot, Israel
Katya Rechav, The Weizmann Institute of Science, Rehovot, Israel
Tamar Unger, The Weizmann Institute of Science, Rehovot, Israel
James L. Van Etten, University of Nebraska-LincolnFollow
Abraham Minsky, The Weizmann Institute of Science, Rehovot, IsraelFollow

Document Type

Article

Date of this Version

2017

Citation

Milrot E, Shimoni E, Dadosh T, Rechav K, Unger T, Van Etten JL, et al. (2017) Structural studies demonstrating a bacteriophage-like replication cycle of the eukaryote-infecting Paramecium bursaria chlorella virus-1. PLoS Pathog 13(8): e1006562.

https://doi.org/10.1371/ journal.ppat.1006562

Comments

Copyright: © 2017 Milrot et al. This is an open access article distributed under the terms of the Creative Commons Attribution License,

Abstract

A fundamental stage in viral infection is the internalization of viral genomes in host cells. Although extensively studied, the mechanisms and factors responsible for the genome internalization process remain poorly understood. Here we report our observations, derived from diverse imaging methods on genome internalization of the large dsDNA Paramecium bursaria chlorella virus-1 (PBCV-1). Our studies reveal that early infection stages of this eukaryotic- infecting virus occurs by a bacteriophage-like pathway, whereby PBCV-1 generates a hole in the host cell wall and ejects its dsDNA genome in a linear, base-pair-by-base-pair process, through a membrane tunnel generated by the fusion of the virus internal membrane with the host membrane. Furthermore, our results imply that PBCV-1 DNA condensation that occurs shortly after infection probably plays a role in genome internalization, as hypothesized for the infection of some bacteriophages. The subsequent perforation of the host photosynthetic membranes presumably enables trafficking of viral genomes towards host nuclei. Previous studies established that at late infection stages PBCV-1 generates cytoplasmic organelles, termed viral factories, where viral assembly takes place, a feature characteristic of many large dsDNA viruses that infect eukaryotic organisms. PBCV-1 thus appears to combine a bacteriophage-like mechanism during early infection stages with a eukaryotic-like infection pathway in its late replication cycle.

Author summary -- Although extensively studied, the mechanisms responsible for internalization of viral genomes into their host cells remain unclear. A particularly interesting case of genome release and internalization is provided by the large Paramecium bursaria chlorella virus-1 (PBCV-1), which infects unicellular eukaryotic photosynthetic chlorella cells. In order to release its long dsDNA genome and to enable its translocation to the host nucleus, PBCV-1 must overcome multiple hurdles, including a thick host cell wall and multilayered chloroplast membranes that surround the host cytoplasm. Our observations indicate that these obstacles are dealt with perforations of the host wall, the host cellular membrane, and the host photosynthetic membranes by viral-encoded proteins. Furthermore, our results highlight a bacteriophage-like nature of early PBCV-1 infection stages, thus implying that this virus uniquely combines bacteriophage-like and eukaryotic-like pathways to accomplish its replication cycle.