1 Molecular Biology Institute, University of California, Los Angeles, CA 90095-1668, USA
2 Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, CA 90095-1668, USA
3 School of Dentistry, University of California, Los Angeles, CA 90095-1668, USA
4 University of Texas Medical School, Department of Microbiology and Molecular Genetics, Houston, TX 77030, USA
5 School of Molecular Biosciences, Washington State University, Pullman, WA 99164-4234, USA
Correspondence
Anthony G. Garza
agarza{at}syr.edu
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ABSTRACT |
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Present address: Department of Biology, Syracuse University, BRL Room 200, 130 College Place, Syracuse, NY 13244-1220, USA.
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INTRODUCTION |
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Although the molecular basis for A-motility is unclear, the cellular components and organelles associated with the S-motility have been studied extensively. S-motility requires functional type IV pili, which are extracellular appendages that localize to the poles of M. xanthus cells (MacRae & McCurdy, 1976; Kaiser, 1979
; Wu & Kaiser, 1995
). It appears that retraction of type IV pili provides the force for S-motility; pili extend outward from the surface of cells, attach to an external substrate, and then retract to pull the cells forward (Kaiser, 2000
; Merz et al., 2000
; Sun et al., 2000
; Skerker & Berg, 2001
). In addition to polar type IV pili, S-motility is dependent on an extracellular matrix of exopolysaccharide (EPS) and protein called fibrils (Arnold & Shimkets, 1988a
, b
; Behmlander & Dworkin, 1994a
; Yang et al., 2000
; Lancero et al., 2002
; Lu et al., 2004
). The fibril matrix provides cohesion between neighbouring cells in multicellular groups, and it helps link cells to the surface substrate (Shimkets, 1986a
; Arnold & Shimkets, 1988a
, b
; Behmlander & Dworkin, 1991
; Ramaswamy et al., 1997
). The results of Li et al. (2003)
suggest that the fibril matrix may serve as an anchoring substrate for type IV pili binding and retraction. In addition to type IV pili and the fibril matrix, wild-type LPS O-antigen is required for S-motility (Bowden & Kaplan, 1998
), although its precise function is unknown.
Relatively little is known about how M. xanthus motility genes are regulated. However, Caberoy et al. (2003) recently uncovered a putative transcriptional activator (Nla24) that is important for gliding motility and fruiting body development. Preliminary morphological studies showed that nla24 cells are unable to swarm on an agar surface, a phenotype that is consistent with defects in both A-motility and S-motility. In the work presented here, we used video microscopy to show that an insertion in the nla24 gene produces a non-motile phenotype on agar plates. This finding suggests that the nla24 gene product plays a novel role in M. xanthus gliding motility; on agar surfaces, Nla24 is absolutely required for A-motility and S-motility. The results of our studies indicate that the nla24 mutant produces LPS O-antigen and functional type IV pili. However, several lines of evidence indicate that the nla24 mutant is defective for production of the EPS portion of the fibril matrix. Transcription of two genes known to be required for A-motility is reduced significantly in the nla24 mutant background, which is consistent with the idea that nla24 cells are defective for A-motility.
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METHODS |
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Motility assays.
Swarm assays on CYE plates containing 1·5 % (favours A-motility) or 0·4 % agar (favours S-motility) were performed as described previously (Shi & Zusman, 1993). Briefly, aliquots (5 µl) of 5x109 cells ml1 were spotted on CYE plates, the plates were incubated for 5 days at 32 °C, and colony-edge morphologies were observed with the x10 objective lens of a Leica inverted phase-contrast microscope. To examine the gliding motility and reversal frequencies of individual cells and groups of cells, overnight cultures were diluted into TPM buffer to about 2x105 cells ml1, and aliquots (5 µl) of the cell suspensions were placed on CYE plates containing 1·5 or 0·4 % agar. Cells were observed using the x32 objective lens of a Leica inverted microscope. Images were captured with a Hyper HAD video camera (Sony) and an AG6040 time-lapse videocassette recorder (Panasonic) as described by Sun et al. (1999)
. Images were observed frame-by-frame to monitor the movements of approximately 100 cells of each M. xanthus strain.
Methylcellulose tethering assays.
Pili function was analysed using tethering assays (Sun et al., 2000). M. xanthus cells were placed in polystyrene culture plates containing 1 % methylcellulose in MOPS buffer (10·0 mM MOPS and 8·0 mM MgSO4, final pH 7·6). Approximately 100 cells of each test strain were observed for 1 h using the x32 objective lens of a Leica inverted microscope. Twenty-sixty per cent of the piliated cells tethered to the surface of the polystyrene plates, whereas non-piliated cells failed to tether to the surface of the plates. Serial digital images of tethered cells were taken at 30 s intervals using a Spot camera (Diagnostic Instruments), and the motion of tethered cells was monitored to determine whether their pili retracted. Since non-tethered cells settled to the bottom of the polystyrene culture plates, we used the above procedure to examine the surface motility and reversal frequency of individual cells under these assay conditions.
LPS analysis.
LPS was isolated from 10 ml volumes of exponentially growing liquid cultures of M. xanthus cells using the modified hot phenol/water method (Apicella et al., 1994). Approximately 15 µg of each preparation was separated by electrophoresis through a deoxycholate (DOC)15 % polyacrylamide gel (Laemmli, 1970
), and visualized by silver staining (Tsai & Frasch, 1982
).
Calcofluor white binding assays.
To detect fibril EPS, calcofluor white binding assays (Ramaswamy et al., 1997) were performed. M. xanthus cells were grown in CYE broth until they reached a density of 5x108 cells ml1, the cells were pelleted by centrifugation, the supernatant was removed, and the cells were resuspended in TPM buffer to a density of 5x109 cells ml1. Aliquots (5 µl) of the cell suspension were spotted onto CYE plates containing 50 µg ml1 of calcofluor white, a fluorescent dye that binds fibril EPS. The cells were incubated for 5 days at 32 °C, and calcofluor white binding was qualitatively determined by exposing the colonies to long-wavelength UV light.
Congo red and Trypan blue binding assays.
To determine the relative levels of fibril EPS, Congo red and Trypan blue binding assays were performed as described by Black & Yang (2004). Briefly, M. xanthus cells were grown in CYE broth until they reached a density of 5x108 cells ml1, the cells were pelleted, the supernatant was removed, and the cells were resuspended in TPM buffer to a density of 5x108 cells ml1. Aliquots of the cell suspensions were mixed with stock solutions of Congo red (150 µg ml1) and Trypan blue (100 µg ml1), dyes that bind to fibril EPS. TPM buffer was added to the cell/dye mixtures to give final concentrations of 2·5x108 cells ml1 and either 15 µg Congo red ml1 or 10 µg Trypan blue ml1. Cell-free samples containing TPM buffer and 15 µg Congo red ml1 or 10 µg Trypan blue ml1 were used as controls. All samples were vortexed briefly and incubated in a 25 °C dark room for 30 min. Following the incubation, the cells were pelleted, and the supernatants were transferred to cuvettes. The absorbance of each supernatant sample was measured at 490 nm to detect Congo red or at 585 nm to detect Trypan blue, and these values were compared to the absorbance of the appropriate control sample. Each test sample and control sample was analysed four times.
Agglutination assays.
The cohesion of M. xanthus cells was measured using the Wu & Kaiser (1997) modifications to the agglutination assay developed by Shimkets (1986b)
. To perform the agglutination assays, cells were grown in CYE broth until they reached a density of approximately 5x108 cells ml1. Aliquots (800 µl) of the cell cultures were placed into cuvettes, and the turbidity of the cells in the cuvettes was monitored for about 2 days by measuring the optical density (600 nm) at various times.
Real-time quantitative RT-PCR.
Aliquots (5 µl) of 5x109 cells ml1 were spotted onto CYE plates, the plates were placed at 32 °C, and cells were harvested at regular intervals during a 3 day incubation period. Total cellular RNA was isolated from 108 cells ml1, and cDNA was generated from the RNA samples using reverse transcriptase (Invitrogen) and random hexamers. Aliquots (4 µl) of the cDNA synthesis reactions were used for the subsequent PCR amplification reactions. PCR reactions contained gene-specific forward and reverse primers (10 µM) and the iQ SYBR Green Supermix (Bio-Rad). The primers were designed to yield approximately 100 bp PCR products. Real-time quantitative RT-PCR was performed using the iCycler iQ system from Bio-Rad. The rate of accumulation of PCR-generated DNA was measured by continuous monitoring of SYBR Green I (Molecular Probes) fluorescence. To confirm that RNA samples were not contaminated with residual genomic DNA, control cDNA synthesis reactions that lacked reverse transcriptase were performed, and the synthesis reactions were analysed using real-time RT-PCR as described above for the test samples. Expression of each motility gene was normalized to that of 16S rRNA, and the relative expression levels in nla24 cells were compared to expression levels in wild-type cells. Similar results were observed when motility gene expression was normalized to the constitutively expressed recA gene.
Western blot analyses.
To detect proteins in whole-cell lysates, aliquots (5 µl) of 5x109 cells ml1 were spotted onto CYE plates, the plates were placed at 32 °C, and cells were harvested at regular intervals as described above for the real-time RT-PCR studies. Approximately 108 cells ml1 were pelleted, and then resuspended in protein lysis buffer containing SDS as described previously by Sun et al. (1999). Samples were electrophoresed through a 12 % polyacrylamide gel, and transferred to an Immobilon P membrane (Millipore) using a semi-dry blotting apparatus. The blots were probed with anti-PilA, anti-DifA, anti-DifD or MAb2105 anti-FibA (Behmlander & Dworkin, 1994b
) antibodies, followed by incubation with peroxidase-conjugated goat anti-rabbit or goat anti-mouse immunoglobulin G (Boehringer Mannheim). The blots were developed with the Renaissance Chemiluminescence Reagent (NEN Life Science Products) and Amersham autoradiography Hyperfilm-MP. Cell-surface pili were isolated using the procedure described by Wall et al. (1998)
. Briefly, M. xanthus cells were harvested from plates and placed in 400 µl TPM buffer. Pili were sheared off the cells by vortexing the cell suspension for 2 min, and the cells were separated from the sheared pili by a room temperature centrifugation at 16 000 g for 5 min. The supernatant was collected, and MgCl2 was added to a final concentration of 100 mM to precipitate the pilus filaments. After 1 h incubation on ice, pilus aggregates were collected by a 4 °C centrifugation at 16 000 g for 20 min. The supernatant was removed, the pilus aggregates were resuspended in sample buffer, boiled for 5 min, and then subjected to Western blot analysis as described above. Anti-PilA antibody was used as the probe for these studies.
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RESULTS |
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Calcofluor white is a fluorescent dye that binds fibril EPS, and it has been used in other studies to detect fibril EPS on the surface of M. xanthus cells (Ramaswamy et al., 1997; Yang et al., 2000
; Black & Yang, 2004
). To determine whether fibril EPS is present on the surface of nla24 cells, they were incubated for 5 days on CYE plates containing calcofluor white, then calcofluor white binding was qualitatively determined by exposing the colonies to long-wavelength UV light. No fluorescence was detected for the nla24 mutant colonies (Fig. 3
), suggesting that the nla24 mutant produces little or no fibril EPS. Similar results were observed when two mutants (difA and difE) known to be defective for production of fibril EPS (Yang et al., 1998
, 2000
) were subjected to calcofluor white binding assays (Fig. 3
).
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M. xanthus mutants that are defective for production of fibril EPS do not agglutinate to the same extent as wild-type cells, indicating that fibril EPS facilitates cell cohesion (Arnold & Shimkets, 1988b). When we performed agglutination assays (Fig. 4
) with nla24 mutant cells, we found that they were less cohesive than wild-type cells. However, this defect in cell cohesion appeared to be less severe than the defects of the difA and difE mutants that lack fibril EPS. These findings are consistent with the results of the calcofluor white, Congo red and Trypan blue binding studies, supporting the idea that the nla24 mutant is defective for production of fibril EPS.
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Expression of A-motility genes
As described in the Introduction, little is known about the cellular components and organelles associated with A-motility in M. xanthus. However, two genes, aglU and cglB, that are required for A-motility have been characterized in some detail (Rodriguez & Spormann, 1999; Spormann & Kaiser, 1999
; White & Hartzell, 2000
; Youderian et al., 2003
). To determine whether the nla24 insertion affects expression of A-motility genes, real-time RT-PCR was used to compare expression of aglU and cglB mRNAs in the nla24 mutant cells and wild-type cells. The levels of aglU and cglB mRNAs in the wild-type and nla24 mutant cells were significantly higher than the negative controls. However, the real-time RT-PCR studies revealed that nla24 mutant cells expressed about threefold less aglU and cglB mRNAs than wild-type cells (Table 3
). These results are consistent with the idea that the nla24 mutant has a defect in A-motility.
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DISCUSSION |
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One of the interesting findings from our tethering assays is that the nla24 mutant and the YL777 mutant (aglU difA) move on the surface of polystyrene plates containing 1 % methylcellulose, whereas the YL555 mutant (aglU
pilA) shows no signs of movement under these assay conditions. Our interpretation of this result is that 1 % methylcellulose compensates for the loss of fibril EPS in the nla24 and YL777 mutants, but it fails to compensate for the loss of type IV pili in the YL555 mutant. Sun et al. (2000)
came to a similar conclusion about fibril EPS mutants and type IV pili mutants when they performed tethering assays. The idea that 1 % methylcellulose compensates for the loss of fibril EPS is supported by two findings: nla24 cells become motile when they are placed on an agar surface that has been overlaid with 1 % methylcellulose, and they are unable to move on a polystyrene surface when it is overlaid with CYE instead of 1 % methylcellulose (data not shown).
How does 1 % methylcellulose compensate for a lack of fibril EPS? It has been proposed fibril EPS may function as a lubricant, decreasing friction when S-motile cells move across a solid surface via retraction of type IV pili. Li et al. (2003) suggested that fibrils might also serve as an anchoring substrate for binding and retraction of type IV pili. When agar or polystyrene surfaces are overlaid with 1 % methylcellulose, S-motile cells encounter less friction. Perhaps under these conditions, S-motile cells do not need type IV pili to bind as tightly to the solid surface and/or they do not need a lubricant to facilitate movement.
Little is known about cellular components and organelles associated with A-motility in M. xanthus. However, Wolgemuth et al. (2002) speculated that A-motility might be similar to gliding motility in cyanobacteria. It has been proposed that gliding motility in cyanobacteria is powered by slime extrusion through nozzles located at the cell poles (Hoiczyk & Baumeister, 1998
; Hoiczyk, 2000
). Genetic and behavioural studies have shown that the aglU and cglB genes are required for the normal function of the A-motility system (Rodriguez & Spormann, 1999
; White & Hartzell, 2000
; Youderian et al., 2003
). Recently, Youderian et al. (2003)
found that the products of several A-motility genes, including aglU, have similarity to the Tol proteins of Escherichia coli. This finding suggests that AglU may be part of a transport complex required for A-motility. The product of cglB appears to be a lipoprotein, but its role in A-motility is unknown. In the work presented here, we have shown that expression of both aglU and cglB is reduced significantly in the nla24 mutant, which is consistent with the idea that the nla24 cells are defective for A-motility.
The product of the nla24 gene is likely to be a member of the NtrC family of transcriptional activators (Caberoy et al., 2003). Based on work in a variety of bacterial systems, it appears that the mechanism of transcriptional regulation by the NtrC family of proteins is well conserved (for review, see Xu & Hoover, 2001
). NtrC-like activators bind to DNA sequences that are typically located between 70 and 150 bp upstream of the 12 bp and 24 bp regions of
54 promoter elements, and they help
54-RNA polymerase to form a transcriptionally active, open promoter complex.
Based on its similarity to NtrC-like activators and the results presented here, it seems likely that Nla24 regulates a subset of genes that are required for A- and S-motilities. Which motility genes in M. xanthus are potential targets for Nla24? Lu et al. (2004) found that nla24 is located within the eps gene cluster, and the products of the eps genes appear to be involved in synthesis of fibril EPS. Hence, it seems reasonable to speculate that Nla24 regulates expression of at least some of these eps genes. The fact that expression of epsY is reduced threefold in the nla24 mutant is consistent with this proposal. The results of our expression studies in the nla24 mutant suggest that the A-motility genes cglB and aglU are also potential targets of Nla24. However, further studies will be needed to determine whether Nla24 activates expression of aglU, cglB or eps genes by binding to their respective promoter elements.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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Received 5 June 2004;
revised 25 August 2004;
accepted 25 August 2004.
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