Structure and Function of Hoc—A Novel Environment Sensing Device Encoded by T4 and Other Bacteriophages
<p>Molecular architecture of the T4 head. (<b>A</b>) The native prolate T4 capsid. (<b>B</b>) The isometric mutant capsid. The major capsid protein gp23* shell surface is shown in cyan; gp24* vertices are shown in magenta; Soc subunits are shown in green; Hoc fibers are shown in orange. The gp23*, gp24*, and Soc structures were determined in the previous cryo-EM studies of the isometric [<a href="#B7-viruses-15-01517" class="html-bibr">7</a>] and prolate capsids [<a href="#B2-viruses-15-01517" class="html-bibr">2</a>], whereas the model of the full-length Hoc has been generated for this study. Panels (<b>C</b>,<b>D</b>) show one pentameric gp24* vertex, one vertex-proximal gp23* hexamer, Soc molecules surrounding gp23*, and Hoc in the center of the gp23* hexamer in surface view (<b>C</b>) or in ribbon diagram (<b>D</b>).</p> "> Figure 2
<p>Structural model of the full-length T4 Hoc protein. (<b>A</b>) Model of T4 Hoc generated using AlphaFold. The residue colors are based on the pLDDT values [<a href="#B33-viruses-15-01517" class="html-bibr">33</a>]. The colors range from blue, corresponding to the pLDDT value of 100 (the highest confidence), to red, corresponding to the pLDDT value of 0 (the lowest confidence). (<b>B</b>) The protein chain is rainbow colored from the N-terminus (blue) to the C-terminus (red). (<b>C</b>) Molecular surface colored according to electrostatic potential showing the acidic nature of the Hoc protein. The surface color ranges from red, corresponding to a potential of −5 kT/e<sup>−</sup>, to blue, corresponding to a potential of +5 kT/e<sup>−</sup>. The potential was calculated assuming 0 M concentrations for the +1 and −1 ion species.</p> "> Figure 3
<p>Hoc orientations on gp23* capsomers. (<b>A</b>) Schematic representation of three gp23* hexameric capsomers. The six possible orientations of Hoc in the center of each capsomer is depicted by arrows. (<b>B</b>) Schematic representation showing the gp24* vertex pentamer as a pentagon and an adjacent gp23* hexamer as a hexagon. The gp23* subunits within the hexamer are shown in different colors. The two preferred orientations of Hoc in the hexamer center are shown by arrows. (<b>C</b>) Surface of the gp24* pentamer (magenta) and an adjacent gp23* hexamer. The gp23* subunits are shown in blue, cyan, green, tan, indigo, and gray. Surfaces of Hoc C-terminal domains corresponding to the two preferred orientations are shown in orange and red. (<b>D</b>) Backbone traces of the Hoc C-terminal domain in the two preferred orientations (yellow and red) fitted into the cryo-EM density of the isometric T4 capsid reconstruction (EMDB-8661) (blue mesh). The letters A–F in panels (<b>B</b>,<b>C</b>) represent the major capsid protein (gp23*) subunits of the hexameric capsomer.</p> "> Figure 4
<p>Structure of the T4 Hoc C-terminal domain. (<b>A</b>) Bottom view of the Hoc C-terminal domain (residues 281–376) corresponding to the preferred orientation 1. The polypeptide chain color changes from yellow at the residue 281 to red at the C-terminal residue 376. The sidechains of the residues interacting with the gp23* subunits are shown as sticks. (<b>B</b>) Superposition of the Hoc C-terminal domain in orientation 1 (orange) with the C-terminal domain in orientation 2 (red) and the C-terminal domain derived from the AlphaFold model (blue).</p> "> Figure 5
<p>Structure of the T4 Hoc C-terminal domain attached to the center of a vertex–proximal gp23* hexamer. Different gp23* subunits are depicted in different colors. Panels (<b>A</b>–<b>C</b>) show Hoc C-terminal domain in the preferred orientation 1 (yellow), and panels (<b>D</b>–<b>F</b>) show the same in the preferred orientation 2 (red). The letters A–F in panels A and D represent the major capsid protein (gp23*) subunits of the hexameric capsomer.</p> "> Figure 6
<p>Interactions of Hoc C-terminal domain with the major capsid protein gp23* subunits. (<b>A</b>) Regions Gly<sup>326</sup>-Arg<sup>344</sup> of the six gp23* subunits forming the Hoc binding sites are shown in different colors. The region Val<sup>353</sup>-Tyr<sup>360</sup> of the Hoc protein in the preferred orientation 1 interacting with gp23* is shown in red. This Hoc region includes the following conserved loop: Glu<sup>355</sup>-Ser<sup>356</sup>-Arg<sup>357</sup>-Asn<sup>358</sup>-Gly<sup>359</sup>. The letters A-F in panel A represent the major capsid protein (gp23*) subunits of the hexameric capsomer. (<b>B</b>) The Hoc C-terminal domain in the preferred orientation 1 interacting with the gp23* surface. The polypeptide chain color changes from yellow at the residue 281 to red at the C-terminal residue 376. The side chains of residues involved in Hoc-gp23* interactions are shown as sticks. (<b>C</b>,<b>D</b>) Close views of some of the Hoc-gp23* interactions.</p> "> Figure 7
<p>Alignment of Hoc C-terminal domain sequences. Only the nine most homologous sequences found by Blast and the Hoc C-terminal domains of phages RB69, JS98, Muldoon, RB49, RB43, and 44RR2.8t are shown here. For the complete sequence alignment (including 650 sequences), see <a href="#app1-viruses-15-01517" class="html-app">Supplementary File S1</a>. The residue colors are based on the conservation. The color ranges from gray for the most conserved residues to red for the least conserved residues. The highly conserved Glu<sup>355</sup>-Ser<sup>356</sup>-Arg<sup>357</sup>-Asn<sup>358</sup>-Gly<sup>359</sup> region is delineated by the black rectangle.</p> "> Figure 8
<p>Clustering behavior of T4 phage with and without Hoc. Plaque assays were performed after incubation of Hoc(−) Soc(−) phage with or without the recombinant T4-Hoc or RB49-Hoc at 4 °C. Percentages and fold differences of plaques were calculated by taking the plaque titer of control Hoc(−) Soc(−) phage as 100% (<b>A</b>), or 1 (<b>B</b>). Error bars were determined from quadruplicate assays. * <span class="html-italic">p</span> < 0.05, ** <span class="html-italic">p</span> < 0.01, and *** <span class="html-italic">p</span> < 0.001, one-way ANOVA test.</p> "> Figure 9
<p>The dispersion of T4 heads (capsids) is dependent on Hoc. (<b>A</b>) Purified T4 capsids were incubated in pH 5.6 (lane 1 to 3) or pH 8 (lane 4 to 6) buffers either with or without the recombinant T4 or RB49 Hoc and in the presence or absence of salts. The samples were sedimented at 8000× <span class="html-italic">g</span> for 45 min, and SDS–PAGE analysis of the pellets was performed. (<b>B</b>) The volume of gp23* band from each lane was determined by ImageDoc, and bar graphs were plotted using the pixel values. The volume of gp23* of Hoc(−) head control was considered as 100%. Error bars were determined from duplicate assays. * <span class="html-italic">p</span> < 0.05, one-way ANOVA test.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Hoc Model Building and Refinement
2.2. In Vitro Assembly of Hoc on T4 Phage Capsid
2.3. Plaque Assay to Determine Clustering vs. Dispersion
2.4. Sedimentation Assay to Determine pH Dependent Clustering vs. Dispersion
3. Results
3.1. Model of the T4 Hoc Protein
3.2. Vertex–Proximal Capsomers Showed Preferred Orientations of Bound Hoc
3.3. Structure of the Hoc C-Terminal Domain Attached to the Vertex–Proximal gp23* Hexamers
3.4. Interactions between Hoc C-Terminal Domain and Major Capsid Protein gp23*
3.5. Hoc C-Domain Interactions in Alternative Orientations
3.6. Structural Models of Phage T4 Full-Length Hoc and of Hoc-like Molecules from Other Bacteriophages
3.7. Hoc Facilitates Dispersion of Phage T4 Virion Particles
3.8. Hoc Might Function as an Environmental Sensor
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Hoc-gp23 in Isometric Capsid | Hoc-gp23 in Prolate Capsid | |
---|---|---|
R.m.s. deviations | ||
Bond lengths (Å) | 0.003 | 0.007 |
Bond angles (°) | 0.62 | 0.69 |
Dihedral angles (°) | 4.84 | 13.50 |
Ramachandran plot | ||
Favored (%) | 91.1 | 90.3 |
Allowed (%) | 8.5 | 9.1 |
Disallowed (%) | 0.4 | 0.6 |
Rotamers outliers (%) | 0.67 | 5.53 |
Clashscore | 13.86 | 12.84 |
CCmask | 0.85 | 0.84 |
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Fokine, A.; Islam, M.Z.; Fang, Q.; Chen, Z.; Sun, L.; Rao, V.B. Structure and Function of Hoc—A Novel Environment Sensing Device Encoded by T4 and Other Bacteriophages. Viruses 2023, 15, 1517. https://doi.org/10.3390/v15071517
Fokine A, Islam MZ, Fang Q, Chen Z, Sun L, Rao VB. Structure and Function of Hoc—A Novel Environment Sensing Device Encoded by T4 and Other Bacteriophages. Viruses. 2023; 15(7):1517. https://doi.org/10.3390/v15071517
Chicago/Turabian StyleFokine, Andrei, Mohammad Zahidul Islam, Qianglin Fang, Zhenguo Chen, Lei Sun, and Venigalla B. Rao. 2023. "Structure and Function of Hoc—A Novel Environment Sensing Device Encoded by T4 and Other Bacteriophages" Viruses 15, no. 7: 1517. https://doi.org/10.3390/v15071517