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The Two Motility Systems Ofmyxococcus Xanthus Show Proc. Natl. Acad. Sci. USA Vol. 90, pp. 3378-3382, April 1993 Microbiology The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces (gliding bacterium/swarming/fruiting/video microscopy) WENYUAN SHI AND DAVID R. ZUSMAN Department of Molecular and Cell Biology, 401 Barker Hall, University of California, Berkeley, CA 94720 Communicated by Horace A. Barker, January 8, 1993 (received for review August 26, 1992) ABSTRACT Myxococcus xanthus, a bacterium that forms In this paper, we report that A-motility and S-motility show fruiting bodies, moves by gliding motility utilizing dual motility different selective advantages on different surfaces: A-mo- systems that differ both genetically and morphologically [sys- tility allows cells to move better than S-motility on relatively tem A, having at least 21 genetic loci and moving mainly single firm and dry surfaces, whereas S-motility allows cells to cells, and system S, having at least 10 genetic loci and moving move much better on relatively soft and wet surfaces. These groups (rafts) of cells] [Hodgkin, J. & Kaiser, D. (1979) Mol. results show that, like flagellated bacteria, the dual motility Gen. Genet. 172, 177-191]. In this study, we found that A- and systems in gliding bacteria allow cells to adapt to a variety of S-gliding-motility systems have different selective advantages physiological and ecological environments. on surfaces containing different concentrations of agar. We observed that colonies of A+S- cells (A-motile cells) swarmed better than A-S+ cells (S-motile cells) on relatively firm and MATERIALS AND METHODS dry surfaces (e.g., 1.5% agar). In contrast, colonies of A-S+ Strains and Culture Conditions. M. xanthus strains used in cells swarmed much better than A+S- cells on soft and wet this study are listed in Table 1. M. xanthus cells were grown surfaces (e.g., 0.3% agar). Individual A-motile cells moved at in a medium consisting of casitone (10 g/liter), yeast extract a rate of 2-4 jam/min on 1.5% agar but they barely moved on (5 g/liter), and 8 mM MgSO4 in 10 mM Mops buffer (pH 7.6; 0.3% agar (<0.5 ,um/min); in contrast S-motile cells moved CYE) (24) at 32°C on a rotary shaker at 225 rpm. Sometimes 3-5 times faster on 0.3% agar than on 1.5% agar. Wild-type a less-rich growth medium (CMM) was used, which consists cells with both A- and S-motility systems were able to move well of casitone (5 g/liter), 8 mM MgSO4, and 10 mM Mops buffer over a wide range of surfaces. These results suggest that dual (pH 7.6). CF medium, used for testing fruiting body forma- motility systems enable the myxobacteria to adapt to a variety tion, was prepared as described (25). Different concentra- of physiological and ecological environments and show simi- tions of agar (Difco), agarose (Sigma), and Gel-Gro (ICN) larities in function to the dual motility systems of flagellated were added to the various media (CYE, CMM, or CF) to bacteria such as Vibrio spp. make swarming or fruiting plates. Swarming and Fruiting. For swarming assays, 2 /,u of cells Dual motility systems are common in the microbial world. at a concentration of 1000 Klett units with a red filter (1 x 107 Many flagellated bacteria (e.g., Vibrio and Proteus) are able cells) was added to the center of the swarming plates; to produce two types of flagella under different conditions alternatively, a wooden stick was used to inoculate bacteria (1-6). Most of these bacteria inhabit very complex environ- from the CYE plates on the center ofthe swarming plates. All ments and their multiple motility systems have different swarming plates were incubated at 32°C for 3-4 days. For selective advantages that enable them to adapt to a variety of fruiting, 20 ,ul of cells at 1000 Klett units (2 x 108 cells) was physiological and ecological environments. One of the best added to the fruiting plates and incubated at 32°C for 2-3 understood examples is Vibrio parahaemolyticus. When the days. The morphology ofthe colonies on swarming or fruiting bacterium is grown in liquid, it produces a single sheathed plates was recorded by a video camera (COHU, model polar flagellum that is used for swimming; when grown on a 4815-2000) with a video macrolens. The morphology of the solidified medium, it produces numerous unsheathed lateral edges of colonies was recorded by the same video camera flagella that are responsible for swarming over the solid through a Zeiss microscope (model 47 60 05-9901). The video surface (5, 7-9). images were printed by a video printer (Hitachi VY-50). Myxococcus xanthus is a gliding bacterium that can move Microscopic Observation of Gliding Motility. Gliding mo- on a solid surface without flagella (for recent reviews, see tility on agar surfaces was observed with a Zeiss microscope. refs. 10 and 11). The mechanism of gliding motility is still A designated medium (5 ml) with a designated concentration largely unknown; however, genetic and morphological anal- ofagar was added to a Falcon tissue culture dish (60 x 15 mm; yses suggest that M. xanthus also contains dual motility Becton Dickinson). After the agar solidified, 10 ,ul ofbacterial systems: (i) system A is required for the movement of single cells was added to the center of the plate. After a 30-min cells or small groups of cells (Fig. lj) and has at least 21 incubation, the bacterial behavior was recorded by video genetic loci; (ii) system S is mainly involved in the movement microscopy for further analysis. Due to the slow movement of cells in groups (Fig. lk) and has at least 10 genetic loci of the M. xanthus cells, a time-lapse video cassette recorder (12-14). Although the genes for A- and S-motility (12-17) and (JVC, model BR-9000U) was used. Bacterial movements the cell surface structure related to A- and S-motility (18-22) were recorded at a 120 times slower rate and played back at have been partially characterized, little is known about the normal speed. The bacteria were maintained at ==22°C, unless physiological differences of the two motility systems in M. otherwise indicated. xanthus. 13-Galactosidase Assay of Tn5-lac Transcriptional Fusions to A- or S-Motility Genes. Cells were harvested directly from The publication costs of this article were defrayed in part by page charge the swarming colonies on different surfaces and broken by payment. This article must therefore be hereby marked "advertisement" sonication. The amounts of protein in these extracts were in accordance with 18 U.S.C. §1734 solely to indicate this fact. determined by the BCA protein assay (Pierce). Protein (80 3378 Downloaded by guest on September 26, 2021 Microbiology: Shi and Zusman Proc. Natl. Acad. Sci. USA 90 (1993) 3379 A+ S A+ S A S+ A S 1 .5% agar a b c d 0.3% agar I e f g h 1.5% agar i k 0.3% agar I I m n 0 p FIG. 1. Swarming colonies and morphologies of the edges of colonies on different concentrations of agar. A+S+, DK1622; A+S-, DK1300; A-S+, DK1217; and A-S-, DZF4150. The medium used was CYE medium with 1.5% or 0.3% agar. The cells (2 Al) were inoculated onto the plates (the initial size of the colonies was around 0.2 cm) and incubated at 32°C for 3 days. The diameters of the swarming colonies (a-h) were 1.6, 0.8, 0.6, 0.35, 2.1, 0.5, 1.7, and 0.35 cm, respectively. The approximate dimensions for the edges of colonies presented in the photos are as follows: i and m, 450 um x 340 ,um; j- and n-p, 110 pm x 90 Am. ug) was assayed for /-galactosidase activity, as described by formed much larger swarming colonies on 0.3% agar (Fig. Miller (26). le). However, the swarming ofA+S- cells was lower on 0.3% agar plate (Fig. lf) than on 1.5% agar (Fig. lb). In contrast, RESULTS A-S+ cells showed limited swarming on 1.5% agar (Fig. lc) but greatly expanded swarming on 0.3% agar (Fig. lg). As a M. xanthus Displays Different Swarming Behaviors on Plates control, A-S- cells did not swarm on 0.3% agar either (Fig. Containing Different Concentrations of Agar. As reported lh). Table 2 compares the colony spreading on 0.3% agar to (12-15, 27, 28), when M. xanthus cells were placed on a solid that on 1.5% agar and shows that A+S+ cells spread more on agar plate (1.5% agar) containing abundant nutrients (such as 0.3% agar, A+S- cells spread less on 0.3% agar, and A-S+ CYE medium), the cells grew vegetatively and showed cells spread much more on 0.3% agar. These results illustrate cooperative swarming movements. Wild-type (A+S+) cells that changing the agar concentration from 1.5% to 0.3% moved away from the colony center to form a large swarming causes A-motility to be reduced whereas S-motility is in- colony (Fig. la). Mutants defective in S-motility (A+S- cells) creased. or mutants defective in A-motility (A-S+ cells) also swarmed Fig. 2 shows a detailed study on the effects of agar on 1.5% agar to expand their colonies (Fig. 1 b and c); concentration on A- and S-motility. At low concentrations of however, both ofthem had less swarming than wild-type cells agar (<0.7% agar), cells having only S-motility (A-S+ cells) (ref.
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