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Department of Microbiology, Miami University, 80 Pearson Hall, Oxford, OH 45056, USA
Correspondence
Mitchell F. Balish
BalishMF{at}MUOhio.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A supplementary figure showing speed distributions for motile cells of each species is available with the online version of this paper.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). This surface-adherent organism exhibits the pleomorphy typical of its genus, but is characterized by a prosthecal terminal organelle or attachment organelle at one pole (Balish, 2006). This structure is the site at which adhesins are clustered, enabling the cell to interact productively with host cells (cytadhere). The attachment organelle is the leading end of the cell during gliding motility (Balish & Krause, 2006) and the location of the gliding motor (Hasselbring & Krause, 2007). Gliding appears to be important for spreading from the initial infection site (Jordan et al., 2007). Duplication of the M. pneumoniae attachment organelle at a site adjacent to the existing one accompanies initiation of DNA replication (Seto et al., 2001).
The cytoplasm within the M. pneumoniae attachment organelle lacks DNA, is clear of large particles, and contains a Triton X-100 (TX)-insoluble structure, the electron-dense core (Biberfeld & Biberfeld, 1970), which appears to be connected to an ill-defined network of cytoskeletal filaments present throughout the cell body (Meng & Pfister, 1980; Göbel et al., 1981). Proper assembly of the core is essential for formation of a functional attachment organelle (Krause & Balish, 2004), making the core essential for virulence. The core consists of several subdomains, including a distal terminal button which is probably in direct contact with the attachment organelle tip, a perpendicularly striated double rod, and a proximal complex that includes a bowl-shaped component at the base (Henderson & Jensen, 2006; Seybert et al., 2006). Although studies of M. pneumoniae attachment organelle mutants have led to the identification of many attachment organelle proteins and to the outline of an assembly pathway (Krause & Balish, 2004), how each protein contributes to the structure of the core remains poorly understood.
Mycoplasma gliding is poorly understood compared to other prokaryotic forms of motility. The M. pneumoniae motility mechanism has been addressed through characterization of mutants with differences in colony-spreading phenotypes, resulting in the identification of a moderate number of genes of both known and unknown function (Hasselbring et al., 2006b). In Mycoplasma mobile, a distant relative whose adherence, motility and terminal organelle components are unrelated to those of M. pneumoniae (Miyata, 2005), gliding is proposed to involve the cyclical binding and release by the adhesin Gli349 (Uenoyama et al., 2004) of carbohydrate moieties present on a wide variety of host-cell proteins, including those deposited on the surface of the microscope slide from serum in vitro (Nagai & Miyata, 2006). A similar binding-and-release process might occur in M. pneumoniae, albeit through the use of an unrelated set of adhesins. In support of this hypothesis, the adhesins P30 (Hasselbring et al., 2005) and P1 (Seto et al., 2005a) have both been implicated in gliding motility of M. pneumoniae. Alternative hypotheses have focused on the electron-dense core as the major component of the M. pneumoniae motor, citing differences in fine features of individual M. pneumoniae cores (Henderson & Jensen, 2006) or postulating that the core is capable of twisting within the attachment organelle (Hegermann et al., 2002). Core-centred models require that the morphology of the core would change during motility, such as by shortening or twisting, and one might further predict that organisms with different motile properties would exhibit corresponding differences in the morphology of the core. The ability to distinguish among these models is predicated on an understanding of the relationship between motile properties and attachment organelle features. One approach to the basis for mycoplasma motility is the characterization of relatives of M. pneumoniae that have a similar motility mechanism but differing motility characteristics, thereby constituting a series of ‘naturally occurring mutants’.
Eight species are currently assigned to the M. pneumoniae cluster based on 16S rRNA sequence similarity (Johansson & Pettersson, 2002) and the presence of an attachment organelle that contains a core (Balish & Krause, 2005). Gliding has been described for some of these species, including M. pneumoniae, Mycoplasma genitalium, Mycoplasma gallisepticum and Mycoplasma amphoriforme, while Mycoplasma alvi has been reported to be non-motile (Bredt, 1979; Hatchel et al., 2006). Mean speeds reported in this cluster range from 50 nm s–1 for M. amphoriforme to >300 nm s–1 for M. pneumoniae (Hatchel et al., 2006). Homologues of the M. pneumoniae attachment organelle proteins required for cytadherence and motility are restricted to the M. pneumoniae cluster (Tham et al., 1994; Dhandayuthapani et al., 1999; Papazisi et al., 2002), making it likely that a common fundamental mechanism involving this set of proteins underlies attachment organelle-mediated functions in each of these organisms. For most of these species, detailed analysis of the dimensions of the electron-dense cores has not been performed. Correlating molecular and structural aspects of attachment organelle components with cytadherence and motility-related properties in each species will reveal which components are likely participants in the motility process, directing future research on the mechanistic aspects of mycoplasma gliding motility.
We have therefore examined each species of the M. pneumoniae cluster with respect to gliding motility and, for motile species, the morphological features of attachment organelles and cores. Time-lapse microcinematographic analysis revealed gliding in all species of the M. pneumoniae cluster except M. alvi. However, scanning electron microscopy (SEM) revealed substantial differences in cell and attachment organelle dimensions among all species which, while largely associated with phylogenetic relatedness, correlated poorly with gliding motility characteristics, not supporting a direct role for the core in motility. In addition, SEM revealed evidence of DNA association with the proximal end of the core in most species.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) to mid-exponential phase (phenol red indicator was orange). M. alvi was also grown in a modified SP-4 formulation containing a 1 : 1 mixture of fetal bovine and porcine sera (HyClone) and grown until slightly turbid. Motility stocks were prepared as previously described (Hatchel et al., 2006). For M. testudinis and M. pirum, cells were passaged three to five times in SP-4 broth to enrich for plastic-attached subpopulations prior to further use and analysis.
Phylogenetic tree.
The 16S rRNA sequence for each species was entered into BioEdit Sequence Alignment Editor v. 7.0.5.2 (Hall, 1999) for trimming and neighbour-joining alignment by CLUSTAL_X v. 1.8 (Thompson et al., 1997). The phylogenetic tree was generated from these data by NJPlot (Perrière & Gouy, 1996).
SEM.
SEM was performed as previously described (Hatchel et al., 2006) with minor modifications. Briefly, stocks were grown in 24-well plates containing glass coverslips for 3 h to 1 day before processing. For analysis of TX-insoluble structures, coverslips were incubated for 30 min at 37 °C in a solution containing 2 % TX in TN buffer (20 mM Tris/HCl, pH 7.5, 150 mM NaCl). For DNase treatment, cells were grown for 1–4 days on coverslips before processing. TX extraction was followed by a 30 min incubation with 5 U bovine pancreas DNase I (Sigma-Aldrich) in 500 µl 1x DNase reaction buffer (10 mM Tris/HCl, pH 7.6, 2.5 mM MgCl2, 0.5 mM CaCl2) at room temperature. For RNase A treatment, TX-extracted coverslips were incubated 30 min in 500 µl TE buffer (10 mM Tris/HCl, pH 8.0, 1 mM EDTA) containing 100 µg RNase A (Qiagen). For whole cells, coverslips were fixed 30 min in fixative A (1.5 % glutaraldehyde/1 % formaldehyde/0.1 M sodium cacodylate, pH 7.2; M. pneumoniae, M. genitalium, M. gallisepticum, M. imitans and M. pirum) or fixative B (1 % glutaraldehyde/2 % formaldehyde/0.1 M sodium cacodylate, pH 7.2; M. amphoriforme and M. testudinis). For visualization of TX-insoluble material, fixative A was used for all species. Dehydration, critical-point drying and gold coating were performed as previously described (Hatchel et al., 2006). Images were viewed and captured on a Zeiss (Carl Zeiss) Supra 35 FEG-VP scanning electron microscope operating at 5 kV. Dimensions of whole cells, TX-insoluble structures, and structures following DNase treatment were measured individually using SPOT software (Diagnostic Instruments).
Time-lapse microcinematographic analysis.
Motility sequences were captured as previously described (Hatchel et al., 2006). Briefly, cells were inoculated into chamber slides containing SP-4+3 % gelatin. After 3 h incubation at 37 °C, cells attached to the slide were visualized using a Leica DM IRB inverted microscope (Leica Microsystems). The sample was held at 37 °C in a heated chamber. Twenty-seven consecutive phase-contrast images were taken at appropriate time intervals and later merged using Adobe Photoshop CS version 8.0. The speed of each cell was computed by measuring the distance travelled and dividing it by the duration of movement. Cells moving in fewer than ten frames were scored motile, but were not included in the calculation of mean speed because below this threshold we regarded the speed measurements as unreliable.
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RESULTS |
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; Pitcher et al., 2005), only M. alvi did not attach to glass and exhibit gliding motility, as previously reported (Bredt, 1979). M. alvi did not attach under any conditions we tested, and consequently we were unable to investigate it further. For M. pirum and M. testudinis, only a small minority of the population derived from the initial stocks attached to glass. In these cases, all further studies were performed on plastic-attached subclones. Efforts to enrich for a similar population of M. alvi cells were unsuccessful.
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). Mean speeds ranged from 28 nm s–1 for M. pirum to 2970 nm s–1 for M. testudinis (Table 1; see also Supplementary Fig. S1, available with the online version of this paper). M. testudinis was the fastest, though with the lowest percentage of motile cells. Although cells glided in the direction of the attachment organelle, large-scale cellular movement appeared generally random for most species. However, 
80 % of M. genitalium and M. testudinis cells moved in nearly circular patterns (not shown). There was no relationship between phylogeny and gliding speed.
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). Dimensions of individual attachment organelles and cells (Table 2) were measured.
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), M. imitans (Fig. 2b), M. amphoriforme (Fig. 2c), and M. testudinis (Fig. 2d) exhibited short, wide attachment organelles, with mean lengths from 120 to 150 nm, and widths from 130 to 150 nm (Table 2). The knob was distinct from the shaft in M. gallisepticum and M. amphoriforme, sometimes in M. testudinis, but not in M. imitans. The M. pirum attachment organelle, which also featured a prominent knob, was long, at 250 nm, and moderately wide, at 100 nm (Table 2), and uniquely exhibited three or four parallel striations approximately perpendicular to the long axis (Fig. 2e). M. genitalium (Fig. 2f) and M. pneumoniae (Fig. 2g) had narrow shafts, only 80 nm in width. The M. genitalium structure, at 170 nm, was substantially shorter than that of M. pneumoniae, which at 290 nm was the longest of the cluster, consistent with previously noted differences (Lind et al., 1984). Knobs were indistinct in M. pneumoniae attachment organelles (Fig. 2g). The two species that exhibited circular gliding paths had curved attachment organelles. For M. testudinis, 25 % of attachment organelles were bent (Fig. 2d), whereas 100 % of M. genitalium attachment organelles were curved an average of 2 °±1 ° from the long axis of the cell (Fig. 2f), and the knob, prominent in this species, was off-centre in the direction of this curvature.
Measurements of cell bodies revealed a positive correlation between cell width and attachment organelle width (Table 2). M. pneumoniae and M. pirum cells were distinctly narrow in comparison to the others (Fig. 2e, g; Table 2). In contrast, cell length appeared unrelated to other features (Table 2). M. pneumoniae cells were unique in the prominence of the trailing filament found at the pole opposite the attachment organelle (Fig. 2g). This structure, whose length varied greatly, drove the mean length of the M. pneumoniae cell to 1500 nm (Table 2). M. gallisepticum and M. amphoriforme cell bodies often had a ridge-like feature in the vicinity of the base of the attachment organelle shaft (Fig. 2a, c).
Cell division
We observed SEM fields of cells from each of the seven adherent species of this cluster (Fig. 3) to characterize cells that appeared to be in the process of dividing. Either the appearance of two attachment organelles at the same pole on a single cell or two attachment organelles pointing in different directions was taken to indicate that cell division was in progress. All species except M. imitans (Fig. 3b) were observed to have cells exhibiting one or both of these phenotypes. Dividing M. pirum cells were only found to have attachment organelles at opposite poles (Fig. 3e), and in M. gallisepticum, adjacently paired attachment organelles were not observed (Fig. 3a), suggesting that in these species the new attachment organelle might not form immediately adjacent to the old one as in M. pneumoniae.
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; Hatchel et al., 2006), have been described. Although we previously had difficulty resolving structures in M. gallisepticum (Hatchel et al., 2006), the use of a fresh preparation of TX resulted in consistent observation of core-like structures in all seven species (Fig. 4).
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). However, rod width varied substantially among species, from 30 to 80 nm (Table 3), and the variation correlated well with phylogenetic relatedness. The length of the M. imitans rod (Table 3) is underestimated on account of being variably obscured by the unusual base (see below). The slight difference between the current results and those previously reported for rod width in M. amphoriforme might be due to the use of a different fixative preparation (Hatchel et al., 2006). Terminal button length and width varied somewhat across species, and although the variation appeared unrelated to gliding speed, width appeared to have a phylogenetic component, with M. pneumoniae and M. genitalium exhibiting the narrowest terminal buttons (Table 3). The M. pneumoniae terminal button was frequently difficult to distinguish from the rod (Fig. 4g), as previously described (Hatchel et al., 2006). The M. genitalium rod exhibited a pronounced lateral curvature, and the terminal button was consistently offset in the direction of this curvature (Fig. 4f). Curvature of the electron-dense core was also visible in 25 % of M. testudinis cells, though in this species the curvature was more abrupt and located close to the terminal button (Fig. 4d). Although we could not image the non-adherent M. alvi, it is known to have an electron-dense core (Gourlay et al., 1977).
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). Incubation in buffer alone had no effect, nor did treatment with RNase A (Fig. 4i). Pronase caused loss of all visible structures (data not shown). In M. genitalium (Fig. 4f) and M. amphoriforme (Fig. 4c) the DNase-sensitive material was predominantly filamentous, with some clumpier regions; in M. gallisepticum (Fig. 4a), M. imitans (Fig. 4b), and M. testudinis (Fig. 4d) this mass was mostly nodular, with occasional filaments; and in M. pirum (Fig. 4e) the material had a smooth appearance with some short filaments extending from it. These filaments are consistent with the appearance of loops of DNA that have been locally denuded of protein (Cunha et al., 2001). Taken together, these data are consistent with the identification of the core-associated material as DNA, rendered condensed by treatment with detergent and salt (Cunha et al., 2001), although whether the interaction between the DNA and the core is physiologically relevant is unclear. Treatment with DNase had no significant effects on measurements of other core substructures, except for occasional lengthening of the rod due to its being less obscured.
The dimensions of the exposed bases were highly variable across species (Table 3; Fig. 4). The base of M. pneumoniae was by far the smallest in both length and width. At the other extreme was M. imitans, which had a very large and highly irregularly shaped base (Fig. 4b). The DNase-treated bases of M. gallisepticum and M. imitans consistently had a notch-like feature of irregular orientation (Fig. 4a, b), suggesting that the removal of DNA was equally complete in each species. No relationship between base dimensions and gliding speed or phylogeny was apparent across species. In fact, although attachment organelle morphology generally correlated well with phylogeny, no relationship was detected between gliding speed and any element of attachment organelle morphology.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Its ultrastructure and phylogenetic position suggest that M. testudinis has a mechanistically similar motor to that of its close relatives, but that it and M. mobile have evolved, perhaps under similar unidentified pressures, to glide rapidly. Alternatively, despite its close relatedness to M. pneumoniae and its similar appearance to its relative, M. testudinis might have acquired a different mechanism for motility, perhaps through horizontal gene transfer. However, the absence of a relationship between the motor mechanism and gliding speed is observed in Mycoplasma pulmonis, which appears to have the same gliding machinery as M. mobile (Seto et al., 2005b), despite its mean speed being much slower (Bredt & Radestock, 1977).
Aside from the curvature of the rod in relation to large-scale near-circular movement in M. genitalium and M. testudinis, no measured dimension of the attachment organelle appeared to correlate with gliding characteristics. Curved paths were previously indicated for M. genitalium (Pich et al., 2006). The curvature of these structures is quite different in the two species, with the rod of the M. genitalium core exhibiting a shallow curvature throughout (Fig. 4f), and that of the M. testudinis core, when curved, being sharply bent at a single location (Fig. 4d). Importantly, this curvature is distinct from the bend observed in M. pneumoniae cores in cells that are not attached to the substrate (Henderson & Jensen, 2006). We do not observe this bend under our conditions, as confirmed by high-angle tilt SEM (not shown), perhaps because when attached to the substrate the attachment organelle is under tension.
In no case did we observe cores that were twisted, as predicted by one model (Hegermann et al., 2002). Although the M. pneumoniae core is clearly suggested to have a broad and a narrow side (Regula et al., 2001; Hegermann et al., 2002; Henderson & Jensen, 2006), there was little variation in rod width within any species. The inchworm model, an alternative model for core function during gliding (Henderson & Jensen, 2006), invokes repeated contraction and expansion of the core along its length, which might have been borne out by substantial differences in rod length of cells within a single species. However, except for M. imitans, whose rod was difficult to measure because of obscuration by the large, irregular base, distributions of the length of the terminal button plus the rod were not dramatic. It is possible that the degree of contraction is too small to be measured by our techniques, but also possible that contraction does not occur. Also, observations of gliding cells did not suggest any quantized movement, though the step size could be smaller, or the steps faster, than our ability to detect. The consistency in the dimensions of cores within each species leads us to propose that the electron-dense core, though an important determinant in attachment organelle biogenesis, is not especially dynamic, and not directly involved in motility.
Cell division
Whether or not the electron-dense core has direct involvement in gliding motility, it might well play a direct role in some other process. Its roles in normal attachment organelle formation and adhesin localization in M. pneumoniae are well documented (Krause & Balish, 2004), though other core-lacking mycoplasmas such as M. mobile (Shimizu & Miyata, 2002) form head-like structures that appear to function analogously to attachment organelles. The special relationship between attachment organelle formation and DNA replication in M. pneumoniae might highlight a role for the electron-dense core in coordination between the two events. An increase in the amount of cellular DNA is accompanied by appearance of a second attachment organelle adjacent to the first one in M. pneumoniae, and the distance between the two organelles increases with continually increasing DNA levels (Seto et al., 2001). Furthermore, time-lapse microcinematography of dividing M. pneumoniae cells reveals that a new attachment organelle generally appears adjacent to the old one, and the new one anchors the cell in place while the old one glides away from it (Hasselbring et al., 2006a), resulting in the two structures being present at opposite poles. Finally, in M. gallisepticum, newly synthesized DNA is specifically enriched in a biochemical fraction itself enriched for attachment organelles (Maniloff & Quinlan, 1974). Although it could be artefactual, the physical interaction observed in this study between the cellular DNA and the electron-dense core is intriguing and will be a subject of future studies.
Evolution
Clearly, the electron-dense core and the attachment organelle, as well as gliding motility, were present in the last common ancestor of the M. pneumoniae cluster; these features were presumably conferred by acquisition of the set of cytadherence-associated genes present in M. pneumoniae and its relatives from an unidentified source. The considerable lengths of the M. pneumoniae and M. pirum structures appear to have arisen independently, since the M. genitalium attachment organelle is not much longer than that of M. amphoriforme. Curvature in M. genitalium and M. testudinis also appears to have developed independently, as discussed above. Thus, the progenitor of these species most likely harboured a short, wide attachment organelle like that of M. gallisepticum and M. amphoriforme. As the knob is markedly reduced only in M. pneumoniae, it was probably prominent in the common ancestor. In addition, the trailing filament appears to be unique to M. pneumoniae and therefore unlikely to have been present in the parent species. Finally, the presence of faster gliding only in M. pneumoniae and especially M. testudinis suggests that slower motility was probably ancestral.
M. pneumoniae appears to be the most derived member of its cluster with respect to attachment organelle and other ultrastructural phenotypes. Its speed is not close to that of any of its relatives, and the reduction in the size of the distal elements of the structure is likely an adaptation to an unknown pressure. Numerous proteins involved in gliding are apparently unique to the subclade containing M. pneumoniae and M. genitalium (Hasselbring et al., 2006b), and it is conceivable that some of these proteins are involved in processes special to one or both of these organisms. Thus, extrapolation of M. pneumoniae attachment organelle-related data to other species ought to be applied cautiously. In contrast, M. amphoriforme might be the most primitive, with its slow speed and average dimensions; as such, it might constitute a more general model for attachment organelle function in species of the M. pneumoniae cluster.
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ACKNOWLEDGEMENTS |
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Edited by: C. Citti
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Received 28 August 2007;
revised 5 October 2007;
accepted 11 October 2007.
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  S. R. Bose, M. F. Balish, and D. C. Krause Mycoplasma pneumoniae Cytoskeletal Protein HMW2 and the Architecture of the Terminal Organelle J. Bacteriol., November 1, 2009; 191(21): 6741 - 6748. [Abstract] [Full Text] [PDF]
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R. F. Relich, A. J. Friedberg, and M. F. Balish Novel Cellular Organization in a Gliding Mycoplasma, Mycoplasma insons J. Bacteriol., August 15, 2009; 191(16): 5312 - 5314. [Abstract] [Full Text] [PDF]
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D. Nakane and M. Miyata Cytoskeletal Asymmetrical Dumbbell Structure of a Gliding Mycoplasma, Mycoplasma gallisepticum, Revealed by Negative-Staining Electron Microscopy J. Bacteriol., May 15, 2009; 191(10): 3256 - 3264. [Abstract] [Full Text] [PDF]
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