A promiscuous DNA packaging machine from bacteriophage T4

Zhihong Zhang, Vishal I. Kottadiel, Reza Vafabakhsh, Li Dai, Yann R. Chemla, Taekjip Ha, Venigalla B. Rao

Research output: Contribution to journalArticle

Abstract

Complex viruses are assembled from simple protein subunits by sequential and irreversible assembly. During genome packaging in bacteriophages, a powerful molecular motor assembles at the special portal vertex of an empty prohead to initiate packaging. The capsid expands after about 10%-25% of the genome is packaged. When the head is full, the motor cuts the concatemeric DNA and dissociates from the head. Conformational changes, particularly in the portal, are thought to drive these sequential transitions. We found that the phage T4 packaging machine is highly promiscuous, translocating DNA into finished phage heads as well as into proheads. Optical tweezers experiments show that single motors can force exogenous DNA into phage heads at the same rate as into proheads. Single molecule fluorescence measurements demonstrate that phage heads undergo repeated initiations, packaging multiple DNA molecules into the same head. These results suggest that the phage DNA packaging machine has unusual conformational plasticity, powering DNA into an apparently passive capsid receptacle, including the highly stable virus shell, until it is full. These features probably led to the evolution of viral genomes that fit capsid volume, a strikingly common phenomenon in double-stranded DNA viruses, and will potentially allow design of a novel class of nanocapsid delivery vehicles.

Original languageEnglish (US)
Article numbere1000592
JournalPLoS Biology
Volume9
Issue number2
DOIs
StatePublished - Feb 2011
Externally publishedYes

Fingerprint

Packaging machines
DNA Packaging
Bacteriophage T4
Bacteriophages
bacteriophages
Capsid
Product Packaging
capsid
DNA
packaging
Head
Viruses
Packaging
Genes
Optical Tweezers
Genome
simple proteins
dsDNA viruses
DNA Viruses
Viral Genome

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

Zhang, Z., Kottadiel, V. I., Vafabakhsh, R., Dai, L., Chemla, Y. R., Ha, T., & Rao, V. B. (2011). A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biology, 9(2), [e1000592]. https://doi.org/10.1371/journal.pbio.1000592

A promiscuous DNA packaging machine from bacteriophage T4. / Zhang, Zhihong; Kottadiel, Vishal I.; Vafabakhsh, Reza; Dai, Li; Chemla, Yann R.; Ha, Taekjip; Rao, Venigalla B.

In: PLoS Biology, Vol. 9, No. 2, e1000592, 02.2011.

Research output: Contribution to journalArticle

Zhang, Z, Kottadiel, VI, Vafabakhsh, R, Dai, L, Chemla, YR, Ha, T & Rao, VB 2011, 'A promiscuous DNA packaging machine from bacteriophage T4', PLoS Biology, vol. 9, no. 2, e1000592. https://doi.org/10.1371/journal.pbio.1000592
Zhang Z, Kottadiel VI, Vafabakhsh R, Dai L, Chemla YR, Ha T et al. A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biology. 2011 Feb;9(2). e1000592. https://doi.org/10.1371/journal.pbio.1000592
Zhang, Zhihong ; Kottadiel, Vishal I. ; Vafabakhsh, Reza ; Dai, Li ; Chemla, Yann R. ; Ha, Taekjip ; Rao, Venigalla B. / A promiscuous DNA packaging machine from bacteriophage T4. In: PLoS Biology. 2011 ; Vol. 9, No. 2.
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