|Alternative modes of locomotion in bacteria
Junctional pores in Oscillatoria. These pores are about 14-16 nm in diameter
and their centre-centre spacing is about twice this distance. These pores form a
single row either side of the circumferential junctional furrow. O, helical oscillin
fibrils (8-12 nm diameter); PC, pore-complex; S, s-layer; SS, secreted slime.
Together, the s-layer and oscillin layer form the ‘external layer’. The inner
membrane is hard to see in fully turgid cryofixed cells as it is tightly pressed
against the inner surface of the peptidoglycan layer. In Oscillatoria princeps
large pores (diameter up to 350 nm at base, narrowing to about 50 nm at the
surface, spaced about 400 nm apart centre-centre) also occur further from the
septum on either side. These large pores are lined by cytoplasm and inner
membrane and represent regular perforations in the peptidoglycan layer.
Many bacteria locomote in ways that do not involve flagella. Typically the speeds attained are much lower than in
flagellated types, and often involves gliding over a solid surface. Cyanobacteria, for example, often form filaments or
chains of cells that are capable of gliding across a solid surface, or up and down inside mucilaginous tubes that they
secrete (they may move up and down these tubes according to a circadian rhythm, altering their position in the water
column to access different nutrients in the water column; download a pdf on bacterial motility for more details).
Although common in the prokaryotic world, gliding motility is hard to study and the physical and molecular
mechanisms are only beginning to be worked-out. This article will be periodically updated as new research comes to
light. It is a fascinating topic that ought to attract more research focus, both for knowledge-sake, but also to better
understand microbial ecosystems and to suggest possible useful techniques for use in nano-engineering.
Gliding Motility and Jet Propulsion in Cyanobacteria
Gliding motility occurs in some Gram negative bacteria and mycoplasmas. Cyanobacteria can glide at up to 10 um/s.
The envelope of gliding cyanobacteria consists of the following layers arranged from outside to inside: oscillin layer,
S-layer, outer membrane, periplasm and the inner membrane.
The oscillin layer is a layer of glycoprotein subunits, 8-12 nm in diameter, arranged in helical arrays and is only
found in gliding forms. This possibly functions as a passive screw thread, causing the filament to rotate as it glides.
The periplasm of gliding forms contains helical fibres, 25-30 nm in diameter, with a 30-degree pitch. One model of
their gliding motility relies on surface waves in a proteinaceous layer, such as in the periplasmic fibres in the
periplasm. A second model proposes that slime extruded from junctional pore complexes (JPCs) known to exist
on either side of the cell-cell junction be guided by the oscillin to produce rotation. Certainly, slime is extruded during
Acetobacter xylinum extrudes cellulose from pores and glides at 0.05 um/s. Spirulina also glides and its JPCs are
situated inside the spiral and not in contact with the substratum.
Hormogonia are motile cyanobacterial filaments (chains of cells) that infect plants and establish cyanobacterial-
plant symbioses. These filaments do not rotate. These possess pili and possibly glide by twitching motility.
Synechocystis is a motile unicellular cyanobacteria and this also has 6-8 nm thick pili. Synechococcus swims, but has
no flagella. The method of locomotion in this case is unclear, but may involve surface waves on the cells pushing
against the surrounding fluid (water behaves as a highly viscous fluid on this microscopic scale).
Twitching Motility in Bacteria – Type IV Pili
This form of motility occurs, for example, in Pseudomonas aeruginosa, Neisseria gonorrhoeae and some Escherichia
coli strains. Motility occurs in short, intermittent jerks of a few micrometers. A moist surface is required for twitching
motility and cells must be within several microns of each other. It involves type IV pili, which alternateley extend,
adhere to the substrate, and then contract - pulling the cell along the substrate. The pili are polar, 6nm in diameter
and up to 4 mm long and occur at one or both poles. These pili actively extend and retract. These pili are also
involved in conjugation, bacteriophage infection, biofilm formation and transformation. At least 35 genes are involved
in twitching motility and speeds of up to 1 um/s are attained. Pili, of various types, are also involved in attachment
and invasion of host cells.
Motility in Myxobacteria
Myxobacteria travel in swarms that co-operatively digest macromolecular food, including prey cells and other
bacteria. Myxobacteria aggregate when nutrients become scarce. These aggregations produce multicellular fruiting
bodies that release dormant myxospores. These bacteria have large genomes, that of Myxococcus xanthus, for
example, is some 9.5 Mbp (Mbp = million base pairs). There are two myxococcal gliding systems, the S system or
‘social’ gliding system and the A system or ‘adventurous’ gliding system. The A system operates in single, isolated
cells. Gliding speeds are about 0.4 um/s.
The S system relies upon type IV pili tethering and retraction to pull the cells along. The gliding is smooth and
possibly some pili extend as others retract. The A system operates over drier surfaces and does not require pili.
Chain-like strands (presumably made of protein), grouped into bands, wrapped helically around the cell, occur in the
periplasm. In Myxococcus fulvus, three or more of these chains are combined into ribbons. The subunit rings have
an outer diameter of about 12-16 nm (12.6 to 15.6 nm) joined by elongated linkers 2.8 nm wide and 9.9-11.9 nm
long. The linkers are arranged in two parallel rows, so that there is one pair of linkers between each pair of rings. It
has been suggested that these periplasmic structures could be involved in A-gliding, however, there is no evidence
that they have any role at all in gliding motility and their function remains unknown.
There are over 100 nozzles in the outer membrane at each cell pole. The trailing pole secretes jets of slime from
these nozzles which push the cell along, whilst nozzles at the leading pole remain inactive. Within one minute the
poles may reverse role, with the trailing pole becoming the leading pole as the cell reverses direction. This strongly
suggests gliding motility by jet propulsion as in some cyanobacteria. these may be used in A system gliding.
Myxobacteria apparently glide over moist surfaces by the use of modified flagella consisting only of the basal
complex and hook but no filament. Mutants lacking these structures are immotile (Pate and Shang, 1979). However,
for reasons that I have not yet uncovered in my literature searches, this mode of gliding seems to have been ignored
by more recent literature.
The Cytophaga-Flavobacterium Group
Bacteria of the Cytophaga-Flavobacterium group glide at about 2-4 um/s. The cells may rotate as they glide and
latex spheres bound to the cell surface move along the cell. The proton-motive force is the likely energy source.
Ring-like structures cover the surface of Flavobacterium johnsoniae; are these rotary motors? Fibrils occur within the
cell walls of some species. Goblet-shaped structures occur in the envelopes of Flavobacterium polymorphus. Most of
these bacteria lack pili and polysaccharide extrusion is considered to be an unlikely motility mechanism in this group.
Gliding motility in this group seems to require sulphonolipids in the outer membrane. These are present in
Flavobacterium johnsoniae and other Cytophaga-Flavobacterium group gliders. Upon contact with a surface, more
polar sulphonolipids are produced and an OMP (outer membrane protein) becomes cross-linked to the
peptidoglycan. One model proposes that adhesive OMPs are moved along tracks fixed to peptidoglycan. Other
models propose conveyer belts of polysaccharide or protein fibrils that are exported and imported at different
locations in the cell surface - conveyer-belting along the outer membrane from the export site to the import site.
Another model proposes expansion or contraction of elements in the cytoplasm or periplasm. Another proposes
rotary motors, and yet another waves in the outer membrane.
The Mycoplasmas are wall-less bacteria related to Gram-positive bacteria. They have very small genomes, that of
Mycoplasma genitalium, for example, is 580 kbp kbp = thousand base pairs). Gliding mycoplasmas have a flask or
club-shaped tip (‘head’) that functions as an attachment organelle. This tip leads the gliding cell at 0.1–7 um/s
depending on species. These bacteria possess a cytoskeleton of over 25 different proteins. It is thought that this
cytoskeleton plays a key role in cell locomotion (as the cytoskeleton does in animal cell locomotion).
Crawling with Flagella
It should be noted that flagella can be used for crawling or gliding over a (moist) solid surface as well as for
swimming. Bacteria like Salmonella typhimurium and Escherichia coli will synthesise more flagella for this purpose,
since gliding is more efficient when there are many flagella covering the cell surface (peritrichous flagellation). The
synthesis of extra flagella is triggered when the bacteria sense an increase in viscosity of the surrounding medium.
This crawling movement may give rise to swarming. This is well studied in Proteus, a bacterium which normally
possesses a single polar flagellum (at one end of the cell) and initially grows on agar by forming distinct colonies.
Soon, however, cells at the edge of the colony change: they elongate and become peritrichously flagellated and
crawl away from the colony in groups. These swarming cells may settle and form a new colony, again with short cells,
until when the new colony reaches a certain size, the process repeats and cells swarm again. In this way Proteus will
eventually cover the whole surface of the agar in a petri dish (an efficient way of accessing all the food available!).
In Escherichia coli and Salmonella typhimurium, swarming also results in elongated cells or filaments (up to 50
micrometres long) that are hyperflagellated (have many more flagella than usual). Again these swarmers move as a
colony - the outer layers of a colony switching to swarming spiral outwards whilst the evacuated space in the centre
is filled with new cells. This results in fast colony expansion of up to 3 micrometres per second (about 1 cm per hour).
During this locomotion the flagella bundle together and rotate as a bundle as they normally would in swimming
(however the cells do not tumble at intervals as they do when swimming, but instead appear to reverse direction
when flagella rotation changes sense).
Additionally swarming cells secrete surfactants which act as 'wetting substances', these are possibly
polysaccharides, and these assist movement over the solid surface.
Above: a hyperflagellated filament.