Arch Microbiol (2000) 174 : 11–17
Digital Object Identifier (DOI) 10.1007/s002030000187
MINI-REVIEW
E. Hoiczyk
Gliding motility in cyanobacteria:
observations and possible explanations
Received: 10 February 2000 / Revised: 19 May 2000 / Accepted: 26 May 2000 / Published online: 29 June 2000
© Springer-Verlag 2000
Abstract Cyanobacteria are a morphologically diverse
group of phototrophic prokaryotes that are capable of a
peculiar type of motility characterized as gliding. Gliding
motility requires contact with a solid surface and occurs in
a direction parallel to the long axis of the cell or filament.
Although the mechanistic basis for gliding motility in cyanobacteria has not been established, recent ultrastructural
work has helped to identify characteristic structural features that may play a role in this type of locomotion.
Among these features are the distinct cell surfaces formed
by specifically arranged protein fibrils and organelle-like
structures, which may be involved in the secretion of mucilage during locomotion. The possible role of these ultrastructural features, as well as consequences for understanding the molecular basis of gliding motility in cyanobacteria, are the topic of this review.
Key words Cyanobacteria · Gliding motility · Bacterial
surface proteins · Carbohydrate secretion · Bacterial
organelles
Introduction
Motility is a widely distributed feature among bacteria. In
fact, locomotion appears to be of significant survival
value to microorganisms in their natural habitats. Most
bacteria move by using small rotary motors called flagella
(Macnab 1999), propulsive organelles which so far have
not been found in cyanobacteria (Häder 1987a). Nevertheless, many cyanobacteria are able to translocate over
surfaces with no visible means of locomotion in a process
called gliding (Castenholz 1982). This intrinsically surface-
E. Hoiczyk (✉)
Laboratory of Cell Biology, The Rockefeller University,
1230 York Avenue, New York, NY 10021-6399, USA
e-mail: [email protected],
Tel.: +1-212-3278181, Fax: +1-212-3277880
linked locomotion is also found in various other bacteria,
e.g. myxobacteria, flexibacteria, Chloroflexaceae, Beggiatoaceae and even the mycoplasmas (Burchard 1981).
In comparison to the swimming of flagellated bacteria
(50 µm/s for Vibrio alginolyticus), gliding is relatively
slow, with average speeds of only a few micrometers a
second. Additional characteristics of gliding motility are
the lack of change in cell morphology during locomotion,
the involvement of extracellular slime, and the requirement of a membrane potential rather than ATP as energy
supply (Pate 1988). However, the lack of a plausible locomotive organelle and the occurrence of gliding movements in various organisms has, until now, challenged a
general explanation. Consequently, a number of mechanisms have been proposed that include contractile elements (Halfen and Castenholz 1971), extrusion of slime
(Hoiczyk and Baumeister 1998), rotary motors (Pate and
Chang 1979), sulfonolipids (Abbant et al. 1986), chainlike aggregates (Freese et al. 1997), and anchorage sites of
the cell surface (Lapidus and Berg 1982). In fact, it seems
likely that gliding in different bacteria is based on different mechanisms and that even cyanobacteria use more
than one mechanism. Some unicellular species, like Synechocystis, move when in contact with a surface using a
mechanism termed twitching (Bhaya et al. 1999), a form
of locomotion dependent on the presence of type IV pili
(Wall and Kaiser 1999). Notably, other unicellular
cyanobacteria of the genus Synechococcus are even able
to swim in the absence of flagella (Waterbury et al. 1985).
Although the precise mechanisms of all types of cyanobacterial motility are still unknown, recent work has revealed certain structural and physiological key features.
These include specific secretion processes (Hoiczyk and
Baumeister 1998), certain bacterial organelles (Bhaya
et al. 1999), and distinct surface proteins of the cells (Brahamsha 1996; Hoiczyk and Baumeister 1997). The possible role of these ultrastructural features, as well as consequences for understanding the molecular basis of gliding
motility in cyanobacteria, are discussed in the following.
12
Occurrence of gliding motility in cyanobacteria
Gliding motility of filamentous cyanobacteria appears as
a relatively slow and smooth surface-associated translocation in the direction of the long axis of the filament at
rates of up to 10 µm/s. When unstimulated, the individual
nonpolar filaments tend to move for about 5–8 min in one
direction before they reverse so that the tip of the moving
filament becomes the rear (Castenholz 1982). The net
movement of the filaments is thereby determined by the
frequency of reversals which is modulated by the filaments in response to various environmental stimuli such
as light (Häder 1987b). In cyanobacteria of the family Oscillatoriaceae, translocation is often accompanied by
species-specific revolutions around the long axis of the
filaments, whereas members of the family Nostocaceae
do not rotate during gliding motility (Drews and Nultsch
1962). Nostocaceae, such as Anabaena sp., are capable
of lateral and bending movements; they often glide in a
U-shaped fashion over the substrate. Every part of the
U-shaped filament can thereby spontaneously stop, reverse, bend or bulge so that the whole filament moves in
a nearly unpredictable pattern. Although these movements
are slower than the gliding of the Oscillatoriaceae, Anabaena filaments are, probably as a consequence of this
difference, capable of true steering movements during
phototactic orientations (Nultsch et al. 1979).
According to many observations, gliding movements
of cyanobacteria are always accompanied by a steady secretion of mucilage, which normally covers the entire surface of the filaments and is deposited as a collapsed and
sometimes twisted trail behind the advancing filaments
(Fig. 1). However, if filaments are unable to move because
they are suspended in a liquid or held by a micromanipulator, the slime starts to be actively translocated over the
filament’s surface (Hosoi 1951; Schulz 1955). The same
effect can be observed if the filaments secrete only small
amounts of mucilage not sufficient to promote locomotion
(Hoiczyk and Baumeister 1998).
The control and coordination of movements
Gliding of cyanobacteria is controlled by a number of external stimuli, of which light seems to be the most important (Häder 1987b). While responding to light, the filaments often slow down, stop and reverse, implying that
the locomotory machinery is actively controlled (Drews
1959). This control not only allows the filaments to reverse their direction, but also establishes the polarity of
the filaments during locomotion. The speed with which a
switch of activity propagates from the leading to the trailing end of the filament suggests the involvement of an
electrical process, i.e. a change of electrical potential
(Murvanidze and Glagolev 1982). Support for this idea
comes from the measurement of potential changes and
from the observation that externally applied electrical
fields inhibit photophobic reactions (Häder 1987a and references therein). According to these observations, the involved sensory transduction chain in cyanobacteria starts
at the photosynthetic pigments. These pigments detect a
change in light intensity via a change of the linear electron
transport through the plastoquinone pool. The result is a
change in proton transport across the thylakoid membrane, which modulates the cytoplasmic electric potential.
This process is thought to trigger Ca2+-specific channels
that open during the light-dependent response and allow a
massive Ca2+ influx from the outside of the cell, thus
causing a depolarization of the cytoplasmic membrane.
How this depolarization is linked to the activity of the locomotory machine remains to be established. But the involvement of voltage-gated calcium channels could explain the observed dependence of motility from Ca2+ ions
in cyanobacteria (Abeliovich and Gan 1982). However,
calcium may have additional functions and has been
found to be necessary for the conformation of the surface
fibril-forming protein oscillin in Phormidium uncinatum
(Hoiczyk and Baumeister 1997).
Cellular structures of cyanobacteria
with possible roles in motility
Fig. 1A,B Mucilage secretion in gliding filamentous cyanobacteria. A Light micrograph of a gliding Anabaena variabilis filament.
B Light micrograph of a moving Phormidium uncinatum filament.
During locomotion both species leave an empty mucilaginous tube
behind, which is stained by the India ink particles sticking to the
mucus. Bar 10 µm. (From Hoiczyk and Baumeister 1998 with kind
permission of Elsevier)
Electron microscopy studies of several filamentous cyanobacteria have revealed certain cellular structures which
are only found in motile species and, therefore, are proposed to be involved in the generation of force during
motility. Among these structures are characteristic cell surfaces formed by specifically arranged protein fibrils and
organelle-like structures which may play a role in the secretion of mucilage during locomotion.
13
Structure of the cell wall of gliding cyanobacteria
Electron microscopy studies of the cell wall structure of
gliding filamentous cyanobacteria have shown that all
species possess a very similar gram-negative cell wall architecture (Hoiczyk and Baumeister 1995). In comparison
to other gram-negative bacteria, however, the peptidoglycan layers of cyanobacteria are considerably thicker, ranging from 30 to 700 nm vs about 5 nm in Escherichia coli.
Furthermore, in all rotating species, the gram-negative
cell wall was covered with a complex external layer
(Fig. 2A, B). This external layer was formed by an S-layer
anchored to the outer membrane and an array of parallel,
helically arranged surface fibrils, 8–12 nm in diameter, on
top of the S-layer. In all cases, the orientation of these sur-
face fibrils correlated with the sense of revolution of the
filaments during locomotion, i.e. clockwise in Phormidium sp. (Fig. 2C) and counterclockwise in Oscillatoria
princeps and Lyngbya aeruginosa. There were no indications of longitudinal corrugations or contractions of the
surface fibrils. No other fibrillar structure could be detected within the cell walls of these cyanobacteria, i.e. no
fibrils between the outer membrane and the peptidoglycan
as had been reported earlier (Halfen 1973). This raises the
possibility that these fibrils had originally been mislocalized, an assumption that would explain why the fibrils
could be visualized by direct replicating of the filament’s
surfaces (Halfen 1973). In cyanobacterial species, such as
Anabaena variabilis, which do not rotate during gliding,
no surface fibrils have so far been found. However, recently, another type of fibrillar cell wall structure has been
reported for an Oscillatoria species (Adams et al. 1999).
In this cyanobacterium, no external surface fibrils were
found, but instead much larger fibrillar structures which
were helically arranged between the outer membrane and
the peptidoglycan layer. Individual fibrils had a diameter
of 25–30 nm and showed no signs of peristaltic alterations.
Biochemical composition of the surface fibrils
Fig. 2A–C Structure of the cell wall of the rotating cyanobacterium Phormidium uncinatum. A Cross-section of the cell wall
showing the gram-negative architecture and the complex external
layer composed of an S-layer and the oscillin fibrils. EL External
layer, OF oscillin fibrils, OM outer membrane, P peptidoglycan.
Bar 200 nm. B Longitudinal section of the cell wall. The location
of the junctional pore complex (JPC) organelles are visible as less
dense channel-like structures. Bar 200 nm. C Tangential section of
a motile filament showing the helical, clockwise arrangement of
the oscillin fibrils. Note the absence of any signs of contractions or
longitudinal corrugation of the oscillin fibrils. Bar 250 nm. (From
Hoiczyk and Baumeister 1995 with kind permission of the American Society of Microbiology)
Only the surface fibrils of P. uncinatum have been characterized at the molecular level (Hoiczyk and Baumeister
1997). They consisted of a single protein, termed oscillin,
which is a 646-amino-acid-long glycoprotein (accession
no. AF002131). Analysis of its sequence showed a twodomain structure. A highly repetitive N-terminal domain
formed by multiple repeats of a Ca2+-binding nonapeptide
motif is followed by a short, non-repetitive C-terminal domain. Oscillin shares no similarity with any other known
motor protein and lacks the nucleotide binding motif
(Walker A and B domain) usually found in these proteins.
Instead oscillin shows similarity over its entire length
with SwmA (accession no. U48223), a surface protein of
swimming Synechococcus (Brahamsha 1996), and two
potential ORFs, from Anabaena (hlyA, accession no.
U13767) and Rhodobacter capsulatus (accession no.
TO3518, Vlcek et al. 1997), with unknown functions. So
far, a role in motility has been established only for SwmA.
However, the precise mechanism, with which this protein
is involved in the generation of thrust during swimming is
not well understood (Brahamsha 1996).
The role of oscillin and oscillin-like proteins in gliding
motility is substantiated by studies of non-motile cyanobacteria deficient in these proteins. Non-motile Aphanothece halophytica mutants lacked a high-molecular-weight
glycoprotein similar to oscillin in their cell wall, which
was thought to be involved in motility (Simon 1981).
However, non-motile P. uncinatum filaments had not only
lost their oscillin fibrils, but also lacked the S-layer and
the junctional pore complex organelle (see below), demonstrating the importance of these elements for gliding
motility in cyanobacteria (Hoiczyk and Baumeister 1997).
14
The structure of the junctional pore organelle
Another characteristic feature of the cell wall of gliding
cyanobacteria is the presence of complex organelles,
called junctional pore complexes (JPCs, see Figs. 2B, 3).
Early indication for the existence of such organelles came
from electron microscopy studies of acid-treated isolated
cell walls (Drews and Nultsch 1962). Using this harsh
method, rows or girdles of fine pores, 14–16 nm in diameter, were found in the peptidoglycan layers of more than
two dozen different cyanobacterial species (Guglielmi
and Cohen-Bazire 1982). However, the fact that these
pores did not penetrate the whole multi-layered cyanobacterial cell wall were first thought to contradict their possible role in slime secretion and gliding motility (Castenholz 1982). Recent work has now revealed that these peptidoglycan pores in fact harbor a far more complex and
larger organelle-like structure. In P. uncinatum, the JPC
organelle has a total length of about 70–80 nm and consists of a straight trans-peptidoglycan channel and a terminal outer membrane pore complex 8 nm in diameter
(Fig. 3, Hoiczyk and Baumeister 1998). Overall, the JPC
organelle is long enough to span the entire cell wall and
thereby bypasses the complex, multi-layered gram-negative cell wall of these organisms (Fig. 4B). In contrast to
P. uncinatum, A. variabilis has not only one row of JPC
organelles at each side of every cross-wall but multiple
rows forming girdles. Despite this slightly different arrangement of the pores, however, the architecture of the
JPC organelles remains the same.
In all motile cyanobacteria, the appearance of the JPC
organelles correlates with the ability of the filaments to
move. The JPC organelles are only found in highly motile
filaments. If, after prolonged cultivation, the filaments become non-motile, the organelles disappear, leaving only
the empty trans-peptidoglycan channels behind (Hoiczyk
Fig. 3 Structure of the JPC organelle in Phormidium uncinatum (see Fig. 2B for the location of the pores in the context
of the cell). Isolated outer membrane patch with the ringshaped orifices of the JPC organelles. Bar 150 nm. The inset shows an average of the
isolated outer membrane part
of the JPC organelle. The
length of the particle is 32 nm,
measuring 14 nm at the central
isthmus. (From Hoiczyk and
Baumeister 1995, 1998)
and Baumeister 1995). These non-motile filaments no
longer secrete mucilage but still possess their external
double layer, formed by an S-layer and the oscillin fibrils.
Observation of slime secretion
in gliding cyanobacteria
As described above, gliding motility in cyanobacteria is
always accompanied by the secretion of mucilage (Fig. 1).
However, if the filaments are immobilized, the mucilage
is actively translocated over the surface of the filament. A
similar transportation of mucilage is observed when a filament is not completely ensheathed by slime but instead
secretes smaller amounts of mucilage in the form of discrete bands (Fig. 4A, Hoiczyk and Baumeister 1998). The
pitch and handedness of the slime band translocation corresponds to the arrangement of the oscillin fibrils, which
form the underlying surface of the filament. By applying
a continuous stream of India ink, these thin bands of mucilage can be sheared from the surface of the filament
floating perpendicular in the current (Fig. 4A). As these
slime bands remained attached at their sites of origin, the
rate of elongation can be measured. Although those measurements are not very precise, the rate of elongation and
thereby secretion is about the same as the rate of gliding
(about 3 µm/s). If the flow of India ink is stopped, the
slime bands regain contact with the filament surface and
are again transported helically over the surface, indicating
that the molecular mechanism of slime translocation is
unaffected by the current.
Very similar observations have been made for A. variabilis, a cyanobacterium which does not rotate during
gliding but can bend and move sideways (Hoiczyk and
Baumeister 1998). Examination of the mucilage secretion
of Anabaena during lateral movements showed that slime
secretion occurred exclusively at the concave side of the
15
observed in Anabaena, where the constricted cross-walls
allowed localization of the JPC organelles, even at light
microscopic resolution.
Possible models for gliding motility in cyanobacteria
These observations and the ultrastructure of the cells led
to the proposal of two different models of how cyanobacteria move. According to the first model, cyanobacterial
filaments glide by the generation of small surface waves,
which travel longitudinally or helically along the filament’s surfaces, pushing the cells forward (Halfen and
Castenholz 1971). These surface waves were thought to
be created by the contraction of the specifically arranged
protein fibrils described above. The contraction waves
should then interact either directly with the underlying
substrate or indirectly via the secreted slime to exert the
necessary force. In order to reverse the direction of gliding the origin of wave propagation may shift from one end
of the filament to the other.
In contrast to the contraction-based model, the alternative hypothesis is based on the extrusion of slime, which
should create sufficient power to drive the filaments
(Schulz 1955; Hoiczyk and Baumeister 1998). According
to this model (Fig. 4B), the JPC organelles steadily secrete
mucilage which flows in tight contact with the filament
surface and adheres to the substrate. This adhesion and the
continuous further secretion of mucilage finally causes the
locomotion of the filament. Helically arranged surface
fibrils are only found in rotating cyanobacteria, where they
act as screw-like threads guiding the rotation of the filament. The reversal of movement may result from a
change in the direction of mucilage flow, caused by the alternation of the sets of pores used.
Fig. 4A,B The slime secretion-based model of gliding motility in
cyanobacteria. A Light micrograph of Phormidium uncinatum secreting mucilage only in form of thin bands. Bar 5 µm. B The secretion process based on the ultrastructural data. The JPC organelle is long enough to span the entire gram-negative cell wall
and seems to be the actual site of slime secretion. The slime flows
in tight contact with the surface of the filament formed by the oscillin fibrils. The helical arrangement of the oscillin fibrils thereby
guides the rotation of the filament. Reversals of movement may result from an alternation of the sets of pores used for secretion.
(From Hoiczyk and Baumeister 1998)
curved filament. As in Phormidium, the slime was secreted in the form of multiple thin bands, which were
elongated at the same rate that the filament moved to the
side. If the secretion of the perpendicularly arranged slime
bands ceased, the locomotion of the filament stopped immediately. Reversals of the lateral movements were only
observed when Anabaena started to secrete slime bands at
the opposite, convex flank of the filament. Thereby lateral
movements never occurred without a corresponding lateral secretion of mucilage. In both species, Phormidium
and Anabaena, the mucilage bands originate in close proximity to the cross-walls, where the junctional pores in
these species are located. This correlation could be easily
Open questions regarding
the contraction-based model
Although a contraction-based mechanism offers a plausible explanation of gliding motility, many questions remain. Helically arranged fibrils have been found in several rotating Oscillatoria species (see above), but so far
there isno evidence for longitudinal fibrils in the cell walls
of non-rotating cyanobacteria (Leak 1967). This observation could indicate that motility in these species is either
based on a different mechanism or that the helically
arranged fibrils in rotating cyanobacteria are involved
only in the rotation but not in the locomotion of the filaments. Another unsolved problem is the demonstration of
the postulated contraction waves. Examination of living
and motile filaments with light or acoustic microscopy has
failed to prove the existence of surface waves (Häder and
Hoiczyk, unpublished data). Even though raised areas in
surface replicas of some Oscillatoria strains were interpreted as evidence for contraction waves (Halfen 1973),
these results could not be confirmed in cryo-prepared
cells (Fig. 2C). Moreover, biochemical analysis of the fi-
16
bril-forming protein oscillin in P. uncinatum showed no
similarity with other known motor proteins (see above).
Yet, another unresolved question is the energy supply for
contraction. In general, the proton motive force (PMF) not
ATP is believed to serve as the energy supply. As the PMF
is generated at the cytoplasmic membrane, it must be
transmitted to the contractile fibrils on top of the cell wall.
In Myxococcus xanthus, it has been suggested that such an
energy transduction could work, analogous to the TonB
system in E. coli (Spormann 1999). TonB is a cytoplasmic
membrane protein that mediates the energy-dependent
transport of iron siderophores across the outer membrane
by a PMF-induced conformational change (Moeck and
Coulton 1998). Could a TonB-like protein power the cyanobacterial fibrils? While such a mechanism might work in
the thin and flexible cell walls of M. xanthus, it is hardly
imaginable that it would function in the up to 700-nmthick and rigid cell walls of motile cyanobacteria.
Unsolved problems
of the slime secretion-based model
Although the secretion-based model explains the lack of
fibrils in non-rotating cyanobacteria and the tight coupling of motility and slime secretion, it contains some hypothetical assumptions. Even though newly secreted
slime bands originate at the location of the JPC organelles, there is no direct proof that the pores are the actual
sites of slime secretion. In addition, the model only works
if the cells can control the activity of the pores using only
one set per cell at a time. Although synchronized processes exist in bacteria, i.e. flagellar rotation (Macnab
1999), there is no evidence that the JPC organelles are indeed synchronized. Another problem is how the JPC organelles can secrete slime so forcefully that it moves the
whole filament, albeit the hydration and swelling of the
mucilage during secretion may be an important factor.
Other factors may be the interaction of the slime with the
surface of the filament and the ability of the mucilage to
adhere to different substrates. A further problem is whether
slime secretion is the basis or a physiological consequence of motility. The observation of movements in
Phormidium and Anabaena suggests that slime secretion
is more likely the cause of locomotion. Both cyanobacteria move at the same speed with which they secrete mucilage and more importantly they always move in the opposite direction. These observations imply that the two
processes, slime secretion and motility, are interrelated;
however, it cannot be completely ruled out that secretion
may be a consequence of motility. Finally, while it has
been questioned whether mucilage secretion has the potential to power motility over a longer period, studies of
the bacterium Acetobacter xylinum clearly demonstrate
the efficiency of mucilage secretion powering motility.
Each Acetobacter cell possesses about 50 JPC organellelike pore complexes, which are used for the secretion of
cellulose, a process that directly moves the cells along
(Brown et al. 1976). Although the speed reached by
A. xylinum is slower (0.05 µm/s) than that of cyanobacteria (10 µm/s), it is within the range reported for other unicellular gliders (Halfen 1979) and shows that mucilage secretion is even able to power locomotion in a heterotrophic bacterium.
New approaches to unravel gliding motility
As indicated by the controversy, there is still no clear answer to the simple-sounding question how cyanobacteria
move without any visible organelle of locomotion. Although recent research has helped to identify new structures and processes involved in gliding motility, more experimental evidence is needed in order to solve this puzzle. Modern techniques such as atomic force microscopy
or the tagging of proteins may allow the study of some of
the described elements in greater detail. These data, together with a complete genome sequence of a gliding
(cyano-) bacterium, could open up new and exciting
routes to understanding how this type of locomotion works.
Although these approaches have only begun, it seems reasonable that they will help us in finally solving the mystery of gliding motility in cyanobacteria and other prokaryotes.
Acknowledgements I thank Joseph Glavy and Rudy Oñate, Jr.
for critical reading of the manuscript and I apologize that, due to
limited space, some of the contributions to this field have not been
cited appropriately. This work was in part supported by a postdoctoral grant from the Deutsche Forschungsgemeinschaft (DFG).
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