The Structure of a Filamentous Bacteriophage

Wang, Ying A.; Xiong, Yong; Overman, Stacy A.; Tsuboi, Masamichi; Thomas, George J.

doi:10.1016/j.jmb.2006.06.027

Cited by 98 publications

(94 citation statements)

References 32 publications

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“…It should be important to know if the MCPs of Ligamenvirales are evolutionary related to those of viruses producing filamentous virions and infecting bacteria or eukarya or if the linear structure of these virions is an example of convergent evolution between unrelated viruses (31). To date, we know only the structures of the filamentous ssRNA Tobamovirus tobacco mosaic virus [TMV; (7)] and the ssDNA Inovirus phage fd (32). Interestingly, the structure of the CP from TMV, although mainly made up of a four-helix bundle, has a different fold compared to the MCPs of AFV1 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage

Goulet

Blangy

Redder

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Acidianus filamentous virus 1 (AFV1), a member of the Lipothrixviridae family, infects the hyperthermophilic, acidophilic crenarchaeaon Acidianus hospitalis. The virion, covered with a lipidic outer shell, is 9,100-Å long and contains a 20.8-kb linear dsDNA genome. We have identified the two major coat proteins of the virion (MCPs; 132 and 140 amino acids). They bind DNA and form filaments when incubated with linear dsDNA. A C-terminal domain is identified in their crystal structure with a four-helix-bundle fold. In the topological model of the virion filament core, the genomic dsDNA superhelix wraps around the AFV1-132 basic protein, and the AFV1-140 basic N terminus binds genomic DNA, while its lipophilic C-terminal domain is imbedded in the lipidic outer shell. The four-helix bundle fold of the MCPs from AFV1 is identical to that of the coat protein (CP) of Sulfolobus islandicus rod-shaped virus (SIRV), a member of the Rudiviridae family. Despite low sequence identity between these proteins, their high degree of structural similarity suggests that they could have derived from a common ancestor and could thus define an yet undescribed viral lineage.crystal structure ͉ viral coat proteins ͉ viral lineages ͉ virus evolution

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Section: Discussionmentioning

confidence: 99%

Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage

Goulet

Blangy

Redder

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…Previous structural models for a small number of phages have been obtained by means of X-ray fiber diffraction (15)(16)(17)(18)(19), static solid-state NMR (20,21), and cryo-EM (22). Structural models for the Ff family have been proposed based on the three methods; however, satisfactory resolution was only obtained for the Y21M mutant of the fd phage (17,18,21) (wt fd is related to M13 by one additional mutation, N12D).…”

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confidence: 99%

“…That is, a fivefold rotation of the major coat protein subunit around the virion axis (pentamers) and an approximate 36°rotation relating two successive pentamers [in fd-Y21M a precise 36°rotation was reported; for fd, values of −33.23° (18) and −34.62° (22) were reported]. All studies report that the coat protein is mostly right-handed, curved, α-helical, with a flexible or disordered N terminus.…”

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confidence: 99%

The NMR–Rosetta capsid model of M13 bacteriophage reveals a quadrupled hydrophobic packing epitope

Morag

Sgourakis

Baker

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

115

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Filamentous phage are elongated semiflexible ssDNA viruses that infect bacteria. The M13 phage, belonging to the family inoviridae, has a length of ∼1 μm and a diameter of ∼7 nm. Here we present a structural model for the capsid of intact M13 bacteriophage using Rosetta model building guided by structure restraints obtained from magic-angle spinning solid-state NMR experimental data. The C5 subunit symmetry observed in fiber diffraction studies was enforced during model building. The structure consists of stacked pentamers with largely alpha helical subunits containing an N-terminal type II β-turn; there is a rise of 16.6-16.7 Å and a tilt of 36.1-36.6°between consecutive pentamers. The packing of the subunits is stabilized by a repeating hydrophobic stacking pocket; each subunit participates in four pockets by contributing different hydrophobic residues, which are spread along the subunit sequence. Our study provides, to our knowledge, the first magicangle spinning NMR structure of an intact filamentous virus capsid and further demonstrates the strength of this technique as a method of choice to study noncrystalline, high-molecular-weight molecular assemblies.solid-state NMR | magic-angle spinning | filamentous bacteriophage | structure determination | Rosetta modeling F ilamentous bacteriophage are long, thin, and semiflexible rod viruses that infect bacteria (1, 2). These large assemblies (∼15-35 MDa) contain a circular single-stranded (ss) DNA genome encapsulated in a protein shell. All filamentous phage have a similar life cycle and virion structure despite the relatively high number of strains, with DNA sequence homology varying from almost complete to very little. The unique phage properties make them ideal for a large range of applications such as phage display (3), DNA cloning and sequencing (4, 5), nanomaterial fabrication (6-8), and as drug-carrying nanomachines (9). In addition, filamentous viruses form a variety of liquid crystals driving the development of both theory and practice of softmatter physics (10, 11). Filamentous viruses are also associated with various diseases, e.g., CTXϕ phage in cholera toxin (12) and Pf4 phage in cystic fibrosis (13).Phage belonging to the Ff family (M13, fd, f1) are F-pilusspecific viruses that share almost identical genomes and very similar structures. M13 is a 16-MDa virus having a diameter of ∼7 nm and a length of ∼1 μm. The capsid is composed of several thousand identical copies of a major coat protein subunit arranged in a helical array surrounding a core of a circular ssDNA. The major coat proteins constitute ∼85% of the total virion mass, the ssDNA ∼12%, and all other minor proteins (gp3, gp6, gp7, gp9) that are specific for infection and assembly constitute about 3% of the total virion mass (1, 14).Previous structural models for a small number of phages have been obtained by means of X-ray fiber diffraction (15-19), static solid-state NMR (20, 21), and cryo-EM (22). Structural models for the Ff family have been proposed based on the three methods; however, ...

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“…To illustrate the procedure of 1-D helical symmetry determination, four superimpositions between the original EM (EMD-1240; bateriophage fd coat protein B; Wang et al, 2006) and transformed density maps relating to the four stages are given in Fig. 7.…”

Section: Resultsmentioning

confidence: 99%

A unified convention for biological assemblies with helical symmetry

Tsai¹,

Nussinov²

2011

Acta Crystallogr D Biol Crystallogr

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Assemblies with helical symmetry can be conveniently formulated in many distinct ways. Here, a new convention is presented which unifies the two most commonly used helical systems for generating helical assemblies from asymmetric units determined by X-ray fibre diffraction and EM imaging. A helical assembly is viewed as being composed of identical repetitive units in a one-or two-dimensional lattice, named 1-D and 2-D helical systems, respectively. The unification suggests that a new helical description with only four parameters [n 1 , n 2 , twist, rise], which is called the augmented 1-D helical system, can generate the complete set of helical arrangements, including coverage of helical discontinuities (seams). A unified four-parameter characterization implies similar parameters for similar assemblies, can eliminate errors in reproducing structures of helical assemblies and facilitates the generation of polymorphic ensembles from helical atomic models or EM density maps. Further, guidelines are provided for such a unique description that reflects the structural signature of an assembly, as well as rules for manipulating the helical symmetry presentation.

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The Structure of a Filamentous Bacteriophage

Cited by 98 publications

References 32 publications

Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage

Acidianus filamentous virus 1 coat proteins display a helical fold spanning the filamentous archaeal viruses lineage

The NMR–Rosetta capsid model of M13 bacteriophage reveals a quadrupled hydrophobic packing epitope

A unified convention for biological assemblies with helical symmetry

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