Viral Hijack of Filamentous Surface Structures in Archaea and Bacteria

Abstract

The bacterial and archaeal cell surface is decorated with filamentous surface structures that are used for different functions, such as motility, DNA exchange and biofilm formation. Viruses hijack these structures and use them to ride to the cell surface for successful entry. In this review, we describe currently known mechanisms for viral attachment, translocation, and entry via filamentous surface structures. We describe the different mechanisms used to exploit various surface structures bacterial and archaeal viruses. This overview highlights the importance of filamentous structures at the cell surface for entry of prokaryotic viruses.

Keywords: archaeal virus; archaellum; flagellum; phage; pilus; viral entry.

Figure 1

Comparison of recognition sites of bacterial viruses. Pie chart based on the database introduced [13]. Filamentous surface structures are a comparatively rare recognition site (~7.5% of total). As the database does not distinguish between primary and secondary recognition sites, some phages that use different primary and secondary receptors are included twice (once for each receptor).

Figure 2

Schematic representation of viral interaction with filamentous structures on the surface of bacteria. The scheme represents the surface of a Gram-negative bacterium. From left to right a type IV pilus (Type II secretion), flagellum (Type III secretion) and F-pilus (Type IV secretion) are shown. (Left) Type IV pili consist of pilins (pink), which are N-terminally processed by PilD and inserted at the base of the growing filament with the help of the ATPase PilB. Secretins allow the filament to cross the outer cell membrane. The pilus can undergo circles of extension and retraction with help of the retraction ATPase PilT, which is necessary for twitching motility. Several viruses, such as PP7 are able to bind to the Type IV pili and when the pilus retracts, are pulled towards the cell surface, where they can interact with a secondary receptor on the cell surface (not shown). This structure is not hollow. (Mid) The flagellum is a rotating filament that is responsible for swimming motility in liquid medium. New subunits, flagellins, travel through the hollow filament and are added at the tip. Rotation relies on a proton motive force. Several viruses can attach to the flagellum, such as Chi (orange) with its tail fibers. ΦCb13 and ΦCbK (green) use their head-filaments to attach to the flagellum. In both cases, the active rotation of the filament supports the translocation of the virions along the length of the filament in the direction of the cell surface according to the nut and bolt model. (Right) The F-pilus is encoded by the F sex plasmid and is involved in conjugation. The hollow pilus dynamically extends and retracts to find a potential recipient cell and draw it into direct contact with the donor cell. Several viruses bind to the F-pilus, including members of the Inoviridae, such as M13 and the Leviviridae, such as MS2. M13 binds the tip of the F-pilus, while MS2 binds along the length of the filament. Retraction of the F-pilus pulls MS2 in the F-pilus channel, which leads to the disruption of the virion and disconnection of the F-pilus. The ATPase TraD couples the F-plasmid substrate to the Type IV Secretion machinery. It is required for MS2 gRNA delivery but not for delivery of Qβ gRNA [33,34]. OM, outer membrane. PG, peptidoglycan. IM, inner membrane.

Figure 3

Schematic representation of viral approach of the archaeal cell surface. This schematic is based on the crenarchaeon Sulfolobus. Sulfolobus has a single membrane and a cell wall of S-layer (gray, surrounded by a glycan barrier (light blue, black line indicates height). It displays different filamentous structures at its surface, which all do not have a hollow interior. In green adhesive T4P are shown, which have homology to bacterial T4P. The pilins are N-terminally processed by PibD before they enter the pilus at the cell proximal end. AapF and AapE have homology to the bacterial T4P proteins PilC (inner membrane platform protein) and PilB (the cytosolic assembly ATPase of the motor complex), respectively. SIRV2 (blue) has a rod-shaped virion of ~900 nm in length and it can bind both at the tip and along the length of the pilus with help of its three tail fibers. It is unknown how the virus translocates along the filament to the cell surface. Retraction of archaeal T4P has not been observed. Adhesive pili are also important for infection of the spindle shaped virus SSV (yellow). Sulfolobus also displays thin non-T4P-like filaments at its surface: threads (orange). The icosahedral virus STIV1 (purple) uses its turrets to bind to these threads. One particle can bind multiple threads and virions get entangled in the filaments. It has been hypothesized that a random walk would lead them to the cell surface.