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Myxococcus Xanthus Proc. Nati. Acad. Sci. USA Vol. 76, No. 11, pp. 5952-5956, November 1979 Microbiology Social gliding is correlated with the presence of pili in Myxococcus xanthus (motility/swarming/cell interactions/fimbriae/Myxobacterales) DALE KAISER Department of Biochemistry, Stanford University, Stanford, California 94305 Contributed by A. Dale Kaiser, August 20, 1979 ABSTRACT Myxococcus xanthus, an organism whose mutation in any one of the loci of system S, exhibit (pure) A- motility involves cell interactions, normally bears pili. Myxo- motility. A-S+ mutants, which have a mutation in any one of coccal pili are found only at cell poles, are less than 10 nm in the loci of system A, exhibit (pure) S-motility. A-S- diameter, and may be longer than a cell. Myxococcus has two mutants, basic patterns of cell movement, adventurous (A-motility) and which have a mutation in any locus of system A and a mutation social (S-motility). Pili are found to be completely correlated in any locus of system S, are nonmotile. with the presence of S-motility. (The S-motility pattern has many There is evidence that pili (fimbriae), first reported on groups of cells, almost no single cells, and is governed by a set myxobacteria by MacRae and McCurdy (8), are associated with of genes called system S.) On the other hand, A-motility is in- motility. Many, but significantly not all, motile myxobacteria dependent of piliation. (The A-motility pattern has many single, and other gliding bacteria that have been examined have polar isolated cells and it is governed by a second set of genes called system A.) Electron microscopic examination of more than 40 pili (8-11) and several nonmotile mutants of M. xanthus were genetically different strains shows that all A+S+ (wild-type) and shown to lack them. But if pili are associated with motility, how A-S+ strains have pili, but A+S- and A-S- strains lack them. can there be nonpiliated motile strains? The existence of two Mutations in four different loci belonging to system S were patterns of movement in M. xanthus, controlled by different tested and were found to stop production of pili: the loci sglA, sets of genes, suggested the possibility that pili might be asso- sglB, sglG, and tgl. When brought into contact with tgl+ cells, ciated with only one of the two patterns. The experiments re- cells of a tgl- strain, which lack pili, become phenotypically ported here were designed to test that possibility. S+ produce pili, and become S-motile. Both motility and the prouction of pili are transient when initiated in this way. Thus it appears that pili permit cells that are close to one another to MATERIALS AND METHODS move. Bacteria. The origin and description of strains DK1200- DK1292 may be found in refs. 6 and 7 and of strains Myxobacteria are rod-shaped cells that move by gliding on DK801-DK898 in ref. 12. DZ2 was described by Campos and surfaces, an activity that helps them carry out their primitive Zusman (13). DK1050 is a single-colony isolate of the motile kind of multicellular development (1, 2). When starved, prototype M. xanthus strain FB (14). DK1622 and DK1253SR thousands of cells assemble to form a fruiting body whose shape are A+S+ transductants of DK1217 and DK1253, respectively, is genetically determined (3). Not only when fruiting but also isolated by David Morandi. DK1805, DK1808, DK1811, when growing in the presence of ample nutrient, myxobacteria DK1813, DK1818, and DK1819 are A+S- transductants of the move in multicellular units (4, 5). A thin halo of cells forms at A-S- strains DK1246, DK1251, DK1252, and DK1292, pro- the edge of a colony on agar and this halo continually expands duced by using phage Mx8 grown on the A+S- strain DK1253. outward. When viewed at higher magnification the edge of the A+ transductants were selected by their capacity to glide halo is seen to consist of a single-layer filigree of cells in which through a Millipore membrane filter 150 tm thick with single cells and groups of cells move and reassort (5). The work 0.45-,gm pores. Transductants were picked and purified and to be reported here is aimed at understanding how myxobac- their A-motility was confirmed by microscopic examinations terial cells interact to regulate and coordinate their move- of the halo of cells around single colonies. ment. The general conditions for growth of bacterial cultures, An investigation of more than 100 mutants of Myxococcus transduction, and stimulation have been described (15). The xanthus has revealed that its movement on agar is composed symbol A+ indicates that all loci of system A are wild-type and of two distinct patterns of movement, named A (for adventu- A- indicates that at least one locus in system A is mutant. S+ and rous) and S (for social). In A-motility, single cells move (6), re- S- have analogous meanings for the loci of system S. sulting in a spatial distribution with many single cells. In S- Assay of Pili. Bacterial cultures were grown in 1% casitone/8 motility, isolated cells do not move, but cells that are close to mM MgSO4/10 mM Tris.HCl, pH 7.6/1 mM potassium phos- one another do move (7). The net result is a spatial distribution phate, pH 7.6 (CTT broth) (15) at 250C with rotary shaking to of cells with many clusters and very few isolated single cells (4, cell densities of 1-4 X 108 cells per ml. (Several cultures were 7). The two patterns are governed by different sets of genes: also grown at 330C, but no differences in piliation from 25'C A-motility by one set of 21 loci, called gene system A and S- cultures were noted, except for temperature-sensitive mutants.) motility by another set of 9 loci, called gene system S (6, 7). One The cells were sedimented, the supernatant fluid was poured motility locus, mgl, is necessary for both kinds of movement. off, and the cell pellet was resuspended in 10 mM Tris-HCl, pH Wild-type M. xanthus has both gene systems and shows a 7.6, at a density of 2 X 108 cells per ml. One drop of cell sus- mixture of the two patterns. However, because all but one of pension was placed on a carbon-coated electron microscope grid the motility loci affect either one or the other of the two patterns but not both, by using mutations it is possible to separate the two Abbreviations: A-motility, adventurous movement; S-motility, social patterns from each other. Thus A+S- mutants, which have a movement. 5952 Microbiology: Kaiser Proc. Natl. Acad. Sci. USA 76 (1979) 5953 and cells were allowed to settle and adhere to the carbon for 1-2 Table 1. Piliation of wild-type strains min. The liquid droplet on the grid was washed by addition of Cell ends with several successive drops of the negative stain- 1% uranyl ace- pili* tate mixed with 30 Mg of bacitracin per ml, serving as a Strain Origin Number % spreading agent (16). The stain solution was immediately re- DK801 Soil (Tracy, CA) 28/79 35 moved with blotting paper and the grid was dried in air. Grids DK804 Soil (Yosemite, CA) 44/53 83 were imaged at an electron optical magnification of X12,600 DK805 Soil (Palo Alto, CA) 49/76 65 and the image was viewed through a X10 telescope. Only those DK806 Soil (Merced, CA) 12/33 36 cell ends were scored that were free of adhering extracellular DK813 Soil (South Dakota) 45/74 61 material and for which the quality of staining was such that in DK816 Soil (Ontario, Canada) 20/30 67 the judgment of the observer it could have revealed pili. Each DK854 Soil (St. Louis, MO) 40/69 58 cell end was scored individually because very often cells were DK879 Soil (King City, CA) 16/34 47 joined by one end to a chain or clump of cells or partly over- DK891 Soil (Ames, IA) 79/110 72 lapped the metallic portion of the grid. To the extent that cells DK897 Soil (Maryhill, WA) 17/41 42 adhere to other cells by their piliated ends, the number of pi- DK898 Soil (Fiji) 35/57 61 hated ends will be underestimated. However, nonpiliated cells DZ2 FB (13) 53/98 54 disperse well and offer no problems for counting. Generally, DK1050 FB (From M. Dworkin in 1973) 68/153 44 only piliated strains form clumps but cultures of these strains DK1622 Transduction of DK1217 41/70 58 also contain many free piliated cells. Therefore, enumeration DK1253SR Transduction of DK1253 157/373 42 of cell ends with pili is most accurate at low degrees of piliation * Under "Number" is given a fraction whose numerator is the number and may underestimate the high degrees of piliation. of cell ends with pili and whose denominator is the total number of ends scored. RESULTS fewer than three at the other. The two poles of a cell thus differ Pili of M. xanthus from each other in a way that might be explained by the dif- Fig. 1 shows a piliated cell of M. xanthus, illustrating several ference in their ages. characteristic features. Pili arise from cell ends. Whenever the Pili observed on negatively stained cells from liquid culture anchor point of a pilus in the cell surface was clearly visible in vary in length. Most are around one cell length long,-3-5 the negatively stained image, it was found in the curved region Am-but some pili are at least 10 ttm long.
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