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Article

A Cut above the Rest: Characterization of the Assembly of a Large Viral Icosahedral Capsid

by
Erin R. Reilly
1,†,
Milky K. Abajorga
1,†,
Cory Kiser
1,
Nurul Humaira Mohd Redzuan
1,
Zein Haidar
1,
Lily E. Adams
1,
Randy Diaz
1,
Juliana A. Pinzon
1,
André O. Hudson
1,
Lindsay W. Black
2,
Ru-Ching Hsia
3,
Susan T. Weintraub
4 and
Julie A. Thomas
1,*
1
Thomas H. Gosnell School of Life Sciences, Rochester Institute of Technology, Rochester, NY 14623, USA
2
Department of Biochemistry and Molecular Biology, The University of Maryland School of Medicine, Baltimore, MD 21201, USA
3
Department of Neural and Pain Sciences, University of Maryland Baltimore School of Dentistry, Baltimore, MD 21201, USA
4
Department of Biochemistry and Structural Biology, The University of Texas Health Science Center at San Antonio, TX 78229, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Viruses 2020, 12(7), 725; https://doi.org/10.3390/v12070725
Submission received: 19 June 2020 / Revised: 3 July 2020 / Accepted: 3 July 2020 / Published: 5 July 2020
(This article belongs to the Special Issue Giant or Jumbo Phages)
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Abstract

The head of Salmonella virus SPN3US is composed of ~50 different proteins and is unusual because within its packaged genome there is a mass (>40 MDa) of ejection or E proteins that enter the Salmonella cell. The assembly mechanisms of this complex structure are poorly understood. Previous studies showed that eight proteins in the mature SPN3US head had been cleaved by the prohead protease. In this study, we present the characterization of SPN3US prohead protease mutants using transmission electron microscopy and mass spectrometry. In the absence of the prohead protease, SPN3US head formation was severely impeded and proheads accumulated on the Salmonella inner membrane. This impediment is indicative of proteolysis being necessary for the release and subsequent DNA packaging of proheads in the wild-type phage. Proteomic analyses of gp245- proheads that the normal proteolytic processing of head proteins had not occurred. Assays of a recombinant, truncated form of the protease found it was active, leading us to hypothesize that the C-terminal propeptide has a role in targeting the protease into the prohead core. Our findings provide new evidence regarding the essential role of proteolysis for correct head assembly in this remarkable parasite.
Keywords: Salmonella; giant phage; myovirus; head assembly; prohead protease; proteolytic maturation; mass spectrometry; transmission electron microscopy Salmonella; giant phage; myovirus; head assembly; prohead protease; proteolytic maturation; mass spectrometry; transmission electron microscopy
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MDPI and ACS Style

Reilly, E.R.; Abajorga, M.K.; Kiser, C.; Mohd Redzuan, N.H.; Haidar, Z.; Adams, L.E.; Diaz, R.; Pinzon, J.A.; Hudson, A.O.; Black, L.W.; et al. A Cut above the Rest: Characterization of the Assembly of a Large Viral Icosahedral Capsid. Viruses 2020, 12, 725. https://doi.org/10.3390/v12070725

AMA Style

Reilly ER, Abajorga MK, Kiser C, Mohd Redzuan NH, Haidar Z, Adams LE, Diaz R, Pinzon JA, Hudson AO, Black LW, et al. A Cut above the Rest: Characterization of the Assembly of a Large Viral Icosahedral Capsid. Viruses. 2020; 12(7):725. https://doi.org/10.3390/v12070725

Chicago/Turabian Style

Reilly, Erin R., Milky K. Abajorga, Cory Kiser, Nurul Humaira Mohd Redzuan, Zein Haidar, Lily E. Adams, Randy Diaz, Juliana A. Pinzon, André O. Hudson, Lindsay W. Black, and et al. 2020. "A Cut above the Rest: Characterization of the Assembly of a Large Viral Icosahedral Capsid" Viruses 12, no. 7: 725. https://doi.org/10.3390/v12070725

APA Style

Reilly, E. R., Abajorga, M. K., Kiser, C., Mohd Redzuan, N. H., Haidar, Z., Adams, L. E., Diaz, R., Pinzon, J. A., Hudson, A. O., Black, L. W., Hsia, R.-C., Weintraub, S. T., & Thomas, J. A. (2020). A Cut above the Rest: Characterization of the Assembly of a Large Viral Icosahedral Capsid. Viruses, 12(7), 725. https://doi.org/10.3390/v12070725

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