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Applied and Environmental Microbiology, October 1998, p. 4079-4083, Vol. 64, No. 10
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
A Gliding Bacterium Strain Inhibits Adhesion and
Motility of Another Gliding Bacterium Strain in a Marine
Biofilm
Robert P.
Burchard* and
Maria L.
Sorongon
Department of Biological Sciences, University
of Maryland, Baltimore County, Baltimore, Maryland 21250
Received 10 April 1998/Accepted 31 July 1998
 |
ABSTRACT |
Two species of gliding bacteria were isolated from a marine
biofilm. They were described and identified as members of the genus
Cytophaga. One of them (RB1057) produced an extracellular inhibitor of colony expansion of the other (RB1058). The inhibitor was
characterized as a glycoprotein with an apparent molecular mass of 60 kDa. It inhibited RB1058 adhesion to and gliding on substrata. Motility
and adhesion of several other aquatic gliding bacteria were not
measurably affected by this agent.
| |
TEXT |
In aquatic habitats, much of the
diverse microbial flora is found in biofilms. There is increasing
interest in the structure and biology of these communities (8, 12,
21). It is likely that there is competition for space and
nutrients among biofilm bacteria. Maintenance of individual species on
substrata would be facilitated by the production of antimicrobial
agents such as bacteriocins that target their competitors. In a
biofilm, the same end would be achieved if one species were able to
inhibit the adhesion and/or spreading of a competitor. Such
interspecies interactions, termed ammensalism or bacterial
interference, are likely to be common, but few have been described
previously (for examples, see references 2, 7, 15,
and 17).
The presence of gliding bacteria in aquatic environments (for examples,
see references 4 and 24), their
ability to adhere to various substrata (for example, see reference
6), and the fact that temporary adhesion is a
requisite for function of their motility machinery all suggest that
gliding bacteria are likely to be members of microbial films. During a
study of the role of extracellular polymers in the adhesion and
motility of marine gliding bacteria, we isolated several strains from a
benthic biofilm in an inlet of Buzzards Bay, Mass., on HSM medium
(yeast extract [0.05%], tryptone [0.2%], and marine salts [3%
Instant Ocean], pH 7.5). Serendipitous coculture of two of these
isolates revealed that expansion of the colony margins of RB1058 was
inhibited when it was 
2 mm from the periphery of a colony of RB1057
(Fig. 1). This led to the hypothesis that
the latter produces an extracellular, diffusible inhibitor of adhesion
and/or motility of the former.
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FIG. 1.
Margins of RB1057 (bottom) and RB1058 (top) colonies >2
mm apart and <2 mm apart (left and right panels, respectively).
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Characterization of strains.
Both RB1057 and RB1058 are
obligate aerobes and require marine salts for growth. Temperature
maxima for growth of both strains were 39°C; both grew at 4°C.
Growth rate constants in HSM at 25°C were 1.1 and 1.2 doublings/h for
RB1057 and RB1058, respectively. Extracellular protease(s) was produced
by both; agarase, amylase, cellulase, and chitinase activities were not
detected for either.
Colonies of both strains were pale yellow as viewed by overhead
illumination or transillumination. Absorption spectra of acetone
extracts of colonies from both isolates demonstrated peaks at
481 and
453 nm and a shoulder at 430 nm, typical of a mixture
of carotenoid
pigments (
18). Addition of KOH did not produce
a
bathochromic spectral shift, indicating the absence of flexirubins
(
25). When viewed under oblique lighting against a dark
background,
colonies of these isolates were distinctively iridescent, a
characteristic
of some cytophagas (
1,
1a,
24,
25a). RB1057
demonstrated
red iridescence; RB1058 was green.
The thermal denaturation temperatures of DNA purified from RB1057 and
RB1058 (
22) indicated that both have a moles percent
guanine-cytosine content of 30, in keeping with their tentative
identification as members of the genus
Cytophaga
(
24).
Biochemical characterization of the RB1057 inhibitor.
The
inhibitor was assayed by applying minute droplets of exponential-phase
culture of RB1058 around the periphery of wells in HSM agar plates with
a 20-µl pipetter. Wells were loaded with 50 µl of solutions
containing the inhibitor. After 7 h of incubation at 25°C, the
spots of RB1058 were examined by stereomicroscopy for inhibition of the
centrifugal movement of flares of gliding bacteria (Fig.
2). In determining the titer of the
agent, the lowest concentration that produced detectable inhibition was
termed the effective concentration.
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FIG. 2.
Agar well assay of inhibitor activity. Droplets (<1
µl) of log-phase RB1058 cells were spotted (center) adjacent to a
3-mm-diameter well (lower left) in HSM agar containing the supernatant
of an RB1057 culture and incubated for ~7 h at 25°C.
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The inhibitor was concentrated under N
2 with an Amicon PM10
filter from 10,000 ×
g supernatant fractions of 3-day
static cultures
of RB1057 grown in HSM medium at 25°C. Low-level
activity was
detected in log-phase cultures, too. The concentrate was
clarified
by centrifugation at 100,000 ×
g for 75 min.
The supernatant was
further concentrated and applied to a Q-Sepharose
anion-exchange
column (Pharmacia Hi trap Q; 0.7 by 2.5 cm). The column
was flushed
with 20 ml of 0.05 M NaCl in Tris buffer (0.02 M, pH 7.5)
followed
by a 50 to 200 mM NaCl linear gradient in the same buffer at a
flow rate of 1 ml/min with a Pharmacia fast protein liquid
chromatography
(FPLC) system. Approximately 80% of the well assay
activity was
recovered in fractions 24 to 30, which comprise a 214 nm-absorbing
peak (Fig.
3A). On a sodium
dodecyl sulfate-10% polyacrylamide
gel (
19), the active
fractions resolved as a band with an apparent
molecular mass of 60 kDa
(Fig.
3B). The intensity of staining
of the band from each fraction
correlated with the well assay
activity of that fraction. Analysis of
peak fractions (24 to 30)
by high-performance size exclusion
chromatography with a Zorbax
SE250 column (100 mM NaPO
4
buffer, pH 6.8, mobile phase) yielded
a 60.5-kDa peak in each, the size
of which corresponded to its
well assay titer (data not presented).
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FIG. 3.
(A) FPLC fractionation of 100,000 × g
supernatant fraction of concentrated RB1057 culture supernatant
(10,000 × g) with a 0.05 to 0.2 M NaCl gradient in
0.02 M Tris buffer (pH 7.5). (B) FPLC fractions from a concentrate of
the RB1057 inhibitor run on a sodium dodecyl sulfate-10%
polyacrylamide gel electrophoresis gel and stained with Coomassie blue
(19). Molecular mass standards (in kilodaltons, shown at
left) are in the leftmost lane. Well assay titers are the reciprocals
of the dilutions giving the effective concentrations.
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The isoelectric point of the inhibitor was determined to be 4.9 with
Bio-Rad ampholytes in a polyacrylamide gel with a Bio-Rad
model 111 mini-isoelectric focusing cell. Colorimetric assays
of the
anion-exchange purified material demonstrated the presence
of protein
(Bio-Rad protein assay reagent [
3]) and carbohydrate
(phenol-sulfuric acid assay [
10]) with a mass ratio of
1:1.
Activity was decreased >10-fold by incubation at 70°C for 20 min.
Activity was also lost by incubation at pH 2 and 10 or in 5 M
guanidine-HCl and by periodate oxidation. Amino acid analysis
of the
pooled peak FPLC fractions was performed by the methods
described by
Henderson et al. (
13). The proportion of tryptophan
residues
was determined based on the ratio of absorbance at 294
nm to that at
206 nm (
14,
28) (Table
1).
Edman degradation
revealed that the N terminus of the polypeptide
component is blocked.
Carbohydrate analysis was carried out on FPLC-purified material that
had been hydrolyzed in 4 M HCl at 100°C (
23). The
monosaccharides
were separated with a Dionex high-performance
anion-exchange chromatography-pulsed
amperometric detection system
on a CarboPac PA1 column with 16
mM NaOH solvent for neutral sugars and
150 mM Na-acetate-100 mM
NaOH for acidic sugars. Monosaccharides were
detected with a pulsed
amperometric detector with a gold electrode.
Identifications were
made based on elution times of standard sugars.
The approximate
compositional ratio of monosaccharides in the inhibitor
was determined
from the areas under the peaks in the elution profile
and comparison
with peaks from known molar quantities of standards of
the same
sugars. Five neutral sugars and no acidic sugars were detected
(Table
2).
Biological characterization of the inhibitor.
Since margins of
inhibited colonies increased in thickness, indicative of bacterial
growth, we concluded that inhibition of RB1058 colony spreading was not
the result of antibiotic action (Fig. 1). Additionally, when RB1058 was
cocultured with RB1057, the viability of RB1058 was unaffected. Also,
incubation of the bacteria in concentrated inhibitor (40× effective
concentration) did not affect viability.
Alternatively, the observed inhibition of colony spreading could result
from inhibition of bacterial adhesion to the substratum
or of gliding
motility. In wet mounts, RB1058 cells quickly adhered
to and glided on
both glass surfaces. They pivoted in place on
one pole, a
characteristic of the cytophagas (for example, see
reference
20). To assess the effect of the inhibitor on
bacterial
behavior, we made video recordings of Nomarski microscopic
images.
Dilutions of the inhibitor were considered to be active at
concentrations
at which
50% of previously motile cells were
inhibited from gliding,
defined as translocation parallel to the long
axis of the cell
over a linear distance of >1 cell length. The
presence of the
inhibitor at twice the effective concentration resulted
in back-and-forth
movements parallel to the bacterial long axis
1/2
cell length
in either direction. Adhesion of the affected bacteria
became
more tenuous, and they exhibited shaky, sideways motion.
Kinetics of inhibition of RB1058 motility were examined by
videomicroscopic tracking of bacteria over a 20-min period. At
2.5- or
5-min intervals, translocation of all the bacteria in
a microscopic
field was measured. Those gliding unidirectionally
over a distance of
>1 cell length during a 30-s period were recorded
as motile. At
t0 (within 1 min of addition of the inhibitor
and
preparation of the wet mount), all of the cells observed in the
microscopic field were motile at all concentrations of inhibitor
tested
(Fig.
4). We observed an approximately
exponential loss
of motility over time; the rate of loss increased with
the concentration
of the inhibitor. An apparent decrease in the
tenacity of adhesion
over time was also observed.
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FIG. 4.
Kinetics of inhibition of RB1058 gliding motility by the
RB1057 inhibitor. The percentage of bacteria demonstrating gliding was
determined at the indicated time intervals after addition of the RB1057
inhibitor at various concentrations.  , effective concentration of
the inhibitor;  and  , two and four times effective concentration,
respectively;  , no inhibitor.
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Direct and simple quantitative bacterial adhesion assays employing
microtiter plates have been reported elsewhere (
9,
26).
We
were unable to demonstrate an effect of the inhibitor by a
modification
of the Shea and Williamson assay (
26). As an alternative,
we
developed a microcapillary adhesion assay. Acid-washed, rectangular
cross-section capillaries (0.1-mm path length, 5-µl volume;
Microslides;
Vitro Dynamics Inc.) were loaded with suspensions of
RB1058 in
HSM (
A540 of 0.1) and incubated for 5 min at ambient temperature.
Sterile HSM was then pumped through the
capillary with a peristaltic
pump at a flow rate of 1 ml or 200 capillary volumes/min for 2
min. This left an average of ~30 to 40 bacteria adherent to the
upper and lower capillary surfaces per
microscopic field examined
at ×400 magnification. When the inhibitor
at the effective concentration
or higher was added to the bacterial
suspension prior to capillary
loading, the number of adherent bacteria
after flushing was reduced
by
5-fold.
The effect of the inhibitor on bacteria associated with substrata
having surface wettabilities distinct from that of untreated
glass was
also examined. Glass was derivatized with organosilanes
or was treated
in a muffle furnace at 482°C for 2 h (
6,
11).
Wettability assays were performed by the standard harmonic mean
(SHM)
method in which drop diameters of methanol-water mixtures
on the
surface in question are measured and reduced to a single
number on a 0 to 100 scale of increasing wettability (
11). Gerhart
et al.
(
11) reported a strong linear relationship between the
SHM
value and
P, the combined polar components of solid
surface tension generated
from contact angle measurements.
Videomicroscopy confirmed our
earlier observations (
6);
RB1058 was less firmly adherent to
the derivatized surfaces as the
surface wettability increased.
On
octadecyldimethylaminopropyltrimethoxysilane (ODAPQ; SHM =
16),
the bacteria adhered to the glass rapidly and more firmly
than they did
to untreated glass (SHM = 49). Gliding typically
commenced after a
lag of approximately 5 min; in contrast, no
lag was detectable on
untreated glass. In the presence of inhibitor
at the effective
concentration, the bacteria appeared to adhere
firmly to the
derivatized glass but demonstrated no gliding. Addition
of inhibitor at
four times the effective concentration resulted
in tenuous adhesion,
again characterized by side-to-side shaky
movement, and no
translocation.
On muffled glass (SHM
83), RB1058 adhered weakly but maintained
the capacity to glide. In the presence of the inhibitor
at the
effective concentration, bacteria appeared to be even more
tenuously
adherent and were subject to sidewise dislocation in
response to flow
of the suspending medium. No gliding was observed.
Another manifestation of both the adhesive properties of the cytophaga
cell surface and the gliding motility machinery is
the ability of these
bacteria to bind and translocate microscopic
particles (for example,
see reference
20). At a concentration
of inhibitor
identical to that which effects inhibition of motility
on untreated
glass (i.e., twice the effective concentration),
very limited binding
of 0.38-µm-diameter polystyrene latex microspheres
was observed.
Microspheres that did bind appeared to do so tenuously
and were
translocated on the bacterial surface only briefly before
detaching.
Reversibility of the inhibitory effect was examined by incubating
RB1058 in the presence of inhibitor at 20 times the effective
concentration. After the treated bacteria were subjected to two
cycles
of centrifugation and resuspension in fresh growth medium,
they
demonstrated poor adhesion and no gliding.
The ability of RB1057 to produce this agent may provide it with a
competitive advantage in colonizing substrata. To test this
hypothesis,
we performed mixed-culture experiments under conditions
designed to
approximate the habitat of these bacteria. Sand, oyster
shell, or glass
beads was the substratum submerged in marine salts
with 1/1,000 and
1/100 the nutrient concentration of HSM. In the
HSM/1,000 medium, the
growth rate constant of RB1057 was 0.86;
that of RB1058 was 0.75. Preliminary results indicated that RB1057
has no competitive growth
advantage over RB1058, either on the
substrata tested or in the aqueous
phase in either dilute medium.
We found the inhibitor to be present at
a low level in cultures
of RB1057 growing in HSM/100.
We also assayed the effect of the inhibitor on other aquatic gliding
bacteria from both marine and freshwater habitats by
the agar well
assay and by direct microscopic observation on ODAPQ-derivatized
slides. Neither adhesion nor motility of RB1057, the producer
of the
inhibitor, was detectably affected by the inhibitor at
10 times the
concentration found to block gliding of RB1058. Similarly,
there was no
effect on two other marine cytophagas, one of which
was isolated from
the same biofilm as RB1058, and three freshwater
gliding bacteria
(
Cytophaga sp. strain U67,
Cytophaga johnsonae,
and
Flexibacter columnaris). In the capillary adhesion
assay,
RB1057 and several other gliding bacteria were unaffected by the
inhibitor at
16 times its effective concentration.
The inhibitor's specificity for RB1058 might be explained by the
dissimilarity of its cell surface to that of several other
gliding
bacteria, each of which demonstrates an array of polypeptides
that are
accessible to radioiodination with an immobilized iodination
catalyst
(
27). In contrast, the RB1058 surface has one predominant
surface-exposed ~50-kDa polypeptide (reference
5
and unpublished
results) which may be the target of the inhibitor.
Characterization
of the inhibitor's interaction with this putative
target might
facilitate our understanding of the mechanisms of adhesion
and
motility of this bacterium.
Assuming that the inhibitor is produced in the marine biofilms
inhabited by RB1057, the biosynthetic cost of synthesis and
export of a
60-kDa glycoprotein would be significant and would
argue for a
significant role(s) in the biology of its producer.
If this agent does
indeed function as an inhibitor of adhesion
and motility in such
biofilms, its high molecular weight would
prove advantageous over a
low-molecular-weight secondary metabolite
in that it would more likely
be retained in the proximity of the
producing bacteria by being trapped
within the extracellular polymeric
matrix of the biofilm and by
diffusing relatively slowly through
the biofilm's channels
(
8).
Marine bacteria produce a variety of products with useful properties
(for example, see reference
16). These studies
suggest
that it may be productive to screen other marine biofilm
bacteria
for the production of other antiadhesion agents. A
broad-spectrum
agent might prove useful in the prevention of
biofouling.
| |
ACKNOWLEDGMENTS |
We gratefully acknowledge the contributions of R. Sowder of NCI,
Fort Detrick, in the amino acid analysis and C. A. Bush and W. LaCourse of UMBC's Department of Chemistry and Biochemistry for
assistance with the carbohydrate analysis and the high-performance size
exclusion chromatography, respectively. C. L. Dull, J. Morales, and M.-J. Shih provided expert assistance. Invaluable discussions were
held with D. Creighton and R. Steiner of the Department of Chemistry
and Biochemistry.
This work was supported by contracts from Maryland Sea Grant (R/MP-1)
and the Office of Naval Research (N00014-88-K-0158) to R.P.B.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biological Sciences, UMBC, Baltimore, MD 21250. Phone: (410) 455-2555. Fax: (410) 455-3875. E-mail: burchard{at}umbc.edu.
Present address: Center for Vaccine Development, University of
Maryland School of Medicine, Baltimore, MD 21201.
| |
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Applied and Environmental Microbiology, October 1998, p. 4079-4083, Vol. 64, No. 10
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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