(l to r) Howard Berg, Abhishek Shrivastava, and Pushkar Lele
Bacterial gliding is defined as steady movement over a surface, of bacteria that have neither flagella nor pili. Gliders are present in many bacterial phyla. The physics and biochemistry of gliding is largely mysterious. Flavobacteria, representatives of gliding bacteria from the phylum Bacteroidetes, are amongst the fastest known gliders. Flavobacteria are found in most aquatic and terrestrial environments. In aquatic environments, they often colonize and glide on aquatic animals and organic detritus. They are opportunistic pathogens that cause severe fish diseases. They possess the ability to secrete enzymes that digest complex polysaccharides and proteins. Usually, Flavobacterium johnsoniae cells move on glass along a straight path at speeds of 2-4 µm/sec, but sometimes they exhibit a random back and forth motion. Rarely and transiently, the cells flip over while attached at one pole and very rarely the cells rotate. F. johnsoniae gliding is powered by proton-motive force. The most remarkable feature of F. johnsoniae gliding is the movement of cell-surface adhesins, SprB and RemA. SprB is filamentous. These adhesins move longitudinally down the length of a cell, occasionally shifting positions to the right or the left. Evidently, interaction of the adhesins with a surface causes the cells to glide. The exact function of most of the proteins involved in gliding is still unclear.
The study by Shrivastava A., Lele P. P. and Berg H. C. published in Current Biology, reports the discovery of a novel gliding motor that rotates in place. The authors developed a method to tether gliding F. johnsoniae. They sheared cells to reduce the number and size of SprB filaments and tethered cells to glass by adding anti-SprB antibody. Tethered cells spun about fixed points, mostly counterclockwise. A population study of rotating cells showed that the speed of rotation was ~1 Hz. The torques required to sustain such speeds are large, comparable to those generated by the flagellar rotary motor and some 25 times larger than the torque generated by the F1 ATPase. Polystyrene beads coated with anti-SprB antibody rotated when attached to sheared cells, further confirming the presence of a rotary motor.
The authors studied the response of gliding motors to changes in load. A viscous agent Ficoll was added and rotation speeds of single cells were measured. They found that gliding motors run at constant speed. However, the torque generated by the motors, equal to the viscosity times the viscous drag coefficient times the speed, increased dramatically. A gliding cell has multiple moving SprB filaments, which are likely to move at the same rather than at different speeds. Otherwise, if more than one filament adhered to the substratum, the motors would not work synchronously. In an earlier study, baseplates attached to SprB filaments were observed by cryo-electron tomography. The authors propose a model in which baseplates might interact with the gliding motor to form a molecular rack and pinion which can convert rotation to longitudinal motion. Alternatively, SprB filament could be attached to the motor directly and with an unknown mechanism it might pass from one motor to the next.
Bacterial surface motility is important for colonization, biofilm formation and pathogenicity. Discovery of the gliding motor is a significant advance towards our understanding of surface motility. Bacteria that have this machinery are widespread in our ecosystem and proteins that regulate this motor might be important switches for transition from motile to sessile stage. The catalog of biological rotary motors now contains three motors powered by protonmotive force: the bacterial flagellar motor, the Fo ATP synthase, and the gliding motor.