Hydrodynamics of bacteriophage migration along bacterial flagella

Abstract

Bacteriophage viruses, one of the most abundant entities in our planet, lack the ability to move independently. Instead, they crowd fluid environments in anticipation of a random encounter with a bacterium. Once they 'land' on the cell body of their victim, they are able to eject their genetic material inside the host cell. Many phage species, however, first attach to the flagellar filaments of bacteria. Being immotile, these so-called flagellotropic phages still manage to reach the cell body for infection, and the process by which they move up the flagellar filament has intrigued the scientific community for decades. In 1973, Berg and Anderson (Nature, 245, 380-382) proposed the nut-and-bolt mechanism in which, similarly to a rotated nut that is able to move along a bolt, the phage wraps itself around a flagellar filament possessing helical grooves (due to the helical rows of flagellin molecules) and exploits the rotation of the flagellar filament in order to passively travel along it. One of the main evidence for this mechanism is the fact that mutants of bacterial species such as Escherichia coli and Salmonella typhimurium that possess straight flagellar filaments with a preserved helical groove structure can still be infected by their relative phages. Using two distinct approaches to address the short-range interactions between phages and flagellar filaments, we provide here a first-principle theoretical model for the nut-and-bolt mechanism applicable to mutants possessing straight flagellar filaments. Our model is fully analytical, is able to predict the speed of translocation of a bacteriophage along a flagellar filament as a function of the geometry of both phage and bacterium, the rotation rate of the flagellar filament, and the handedness of the helical grooves, and is consistent with past experimental observations.

The flagellotropic bacteriophage YSD1 targets Salmonella Typhi with a Chi‐like protein tail fibre

“…In YSD1, Chi and Chi‐like phages, YSD1_29 and its homologs form the tail fibre. The hydrodynamic calculations of phage movement along flagellae support a model in which only a counter‐clockwise rotation of the flagellum would promote movement of the phage along the right‐handed groove in the flagellum towards the bacterial cell surface (Katsamba and Lauga, ). The corkscrew shape of the YSD1_29 protein adds further support to this intimate relationship between the phage tail structure and the bacterial flagellum.…”

“…1C) and Chi (Schade et al, 1967). It corresponds to the main element that would need to interact with bacterial flagellae in current theoretical models for engagement of flagellotropic phage with bacteria (Katsamba and Lauga, 2019). Salmonella spp.…”

“…Movement along the bacterial flagellum was first proposed as a nut-and-bolt mechanism (Berg and Anderson, 1973) and has recently been modelled through precise calculations that indicate that speed of travel is determined by factors that include the length of the tail fibre (Katsamba and Lauga, 2019). In Salmonella, counter-clockwise rotation operates for forward swimming, a state in which each flagellum forms a coordinated bundle (Macnab, 1977).…”

The architecture and stabilisation of flagellotropic tailed bacteriophages

“…The head and the tail components of phages have to withstand considerable mechanical stress in the extracellular phase of the viral cycle 7 , perhaps none more so than flagellotropic phages. These phages, such as the archetypal χ phage 8,9 , recognise and engage bacterial flagella before being spun at extraordinary velocity (several microns per second) and shear force towards the bacterial cell surface 10 ( Supplementary Fig. 1).…”

Bacteriophages: Ecological role in the marine environment and potential applications

“…Bacteriophages (phages) are bacteria-specific viruses. They are the most abundant biological entities on earth (Katsamba and Lauga, 2019). They exist in all ecosystems.…”