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Proteus Mirabilis Mutants Defective in Swarmer Celldifferentiation

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Proteus Mirabilis Mutants Defective in Swarmer Celldifferentiation JOURNAL OF BACTERIOLOGY, Oct. 1991, p. 6279-6288 Vol. 173, No. 19 0021-9193/91/196279-10$02.00/0 Copyright © 1991, American Society for Microbiology Proteus mirabilis Mutants Defective in Swarmer Cell Differentiation and Multicellular Behaviort ROBERT BELAS,1,2* DEBORAH ERSKINE,' AND DAVID FLAHERTY1 Center of Marine Biotechnology, The University ofMaryland, 600 East Lombard Street, Baltimore, Maryland 21202,1* and Department ofBiological Sciences, University ofMaryland Baltimore County, Baltimore, Maryland 212282 Received 21 June 1991/Accepted 24 July 1991 Proteus mirabilis is a dimorphic bacterium which exists in liquid cultures as a 1.5- to 2.0-,um motile swimmer cell possessing 6 to 10 peritrichous flagella. When swimmer cells are placed on a surface, they differentiate by a combination of events that ultimately produce a swarmer cell. Unlike the swimmer cell, the polyploid swarmer cell is 60 to 80 ,um long and possesses hundreds to thousands of surface-induced flagella. These features, combined with multicellular behavior, allow the swarmer cells to move over a surface in a process called swarming. Transposon TnS was used to produce P. mirabUis mutants defective in wild-type swarming motility. Two general classes of mutants were found to be defective in swarming. The first class was composed of null mutants that were completely devoid of swarming motility. The majority of nonswarming mutations were the result of defects in the synthesis of flagella or in the ability to rotate the flagella. The remaining nonswarming mutants produced flagella but were defective in surface-induced elongation. Strains in the second general class of mutants, which made up more than 65% of all defects in swarming were motile but were defective in the control and coordination of multicellular swarming. Analysis of consolidation zones produced by such crippled mutants suggested that this pleiotropic phenotype was caused by a defect in the regulation of multicellular behavior. A possible mechanism controlling the cyclic process of differentiation and dedifferen- tiation involved in the swarming behavior of P. mirabilis is discussed. Proteus mirabilis is a motile gram-negative bacterium, proteins, e.g., flagellin (FliC, the product of the fliC gene), similar in many aspects of its physiology to other members the protein subunit of the flagellar filament, is altered mark- of the family Enterobacteriaceae, such as Escherichia coli edly in the swarmer cell (3, 5, 14). The result of this process and Salmonella typhimurium. It was originally described and is a very long, nonseptate, polyploid cell. The number of named by Hauser in 1885 for the character in Homer's chromosomes in the swarmer cell is roughly proportional to Odyssey who "has the power of assuming different shapes in the increase in length, such that a 40-p.m swarmer cell has order to escape being questioned" (quoted from reference about 20 chromosomes (6). Eventually septation and divi- 18). P. mirabilis is considered to be an opportunistic patho- sion do take place at the ends of the long swarmer cells, gen and is one of the principal causes of urinary infections in producing a microcolony of differentiated cells. hospital patients with urinary catheters (32, 34). Its ability to Concurrent with cellular elongation, changes take place in colonize the surfaces of catheters and the urinary tract may the rate of synthesis of flagella on the swarmer cell. Although be aided by the characteristic first described more than a swimmer cells have only a few flagella, the elongated century ago and currently referred to as swarmer cell differ- swarmer cells are profusely covered by hundreds to thou- entiation. sands of new flagella (Fig. 1A) synthesized specifically as a When grown as in suitable liquid media, P. mirabilis exists consequence of growth on the surface (4, 19, 20). The term 1.5- to 2.0-,um to motile cells with 6 10 peritrichous flagella. "flagellin factories" was first used by Hoeniger (19) to These bacteria, called swimmer cells, display characteristic describe the tremendous new swimming and chemotactic behavior, moving toward nutri- synthesis of flagella in swarmer cell differentiation. The newly synthesized surface- ents and away from repellents (36). However, a dramatic induced flagella are composed of the same flagellin subunit change in cell morphology takes place when cells grown in as the swimmer cell flagella, indicating that the same flagellar liquid are transferred to a nutrient medium solidified with species is overproduced upon surface induction (6). The agar. Shortly after encountering an agar surface, the cells result of the surface-induced differentiation process is a begin to elongate. This is the first step in the production of a swarmer cell, which differs from the swimmer cells by morphologically and biochemically differentiated cell, re- having the unique ability to move over solid media in a ferred to as the swarmer cell. The process of elongation translocation process referred to as swarming (17). How- takes place with only a slight increase in cell width and is due ever, individual swarmer cells by themselves do not have the to an inhibition in the normal septation mechanism, although ability to swarm (10). Swarming is the result of a coordi- the molecular mechanism of inhibition is not known. Elon- nated, multicellular effort of groups of differentiated gation of the swarmer cell can give rise to cells 60 to 80 pum swarmer cells (10). The process begins when a group of in length. During this process, DNA replication proceeds differentiated swarmer cells move outwards as a mass and without significant change in rate from that in the swimmer continues until the mass of bacteria is reduced in cell (15). Not surprisingly, the rate of synthesis of certain swarming number as a result of loss of constituent cells which fall behind on the surface or when the mass reverses direction. Swarming of P. mirabilis is cyclic. Once swarmer cells * Corresponding author. have fully differentiated, the swarming colony moves out- t Publication 154 from the Center of Marine Biotechnology. ward in unison from all points along the periphery for a 6279 A FIG. 1. Swarmer cell morphology and swarming motility of P. mirabilis. (A) Electron micrograph of a wild-type swarmer cell taken from the periphery of a swarming colony grown on L agar at 37°C for 6 h and negatively stained with uranyl acetate. Bar, 5 pm. (B) Swarming colony and resulting consolidation patterns of BB2000 grown on an L agar plate at 37°C for 16 h. Oblique lighting directed at the underside of the agar plate was used to accent the consolidation zones, which show up as lighter concentric rings in the swarming colony. 6280 VOL. 173, 1991 PROTEUS MUTANTS DEFECTIVE IN MULTICELLULAR SWARMING 6281 TABLE 1. Strains used in this study Strain Genotype or phenotypea Derivation Referencesource or E. coli CSH4 trp lacZ strA thi recA FliC- Laboratory stock DH5a supE44 supF58 hsdS3 (rB mB ) Laboratory stock dapD8 lacYl gin V44 A(gal- uvrB)47 tyrT58 gyrA29 tonA53 A(thyA57) P. mirabilis PRM1 Wild type J. Shapiro BB2000 Rif Spontaneous from PRM1 7 BB2022 swr-2022::Tn5 Cm Swrcr Elo- pUT/mini-Tn5 Cm x BB2000b This study BB2029 swr-2029::TnS Cm Swrcr pUT/mini-Tn5 Cm x BB2000 This study BB2035 swr-2035::TnS Cm Swr- Mot- pUT/mini-TnS Cm x BB2000 This study BB2040 swr-2040::TnS Cm Swr- Elo- pUT/mini-TnS Cm x BB2000 This study BB2075 swr-2075::Tn5 Cm Swr- Che- pUT/mini-TnS Cm x BB2000 This study BB2076 swr-2076::Tn5 Cm Swr- Eloc pUT/mini-TnS Cm x BB2000 This study BB2105 swr-2105::Tn5 Cm Swrcr Eloc pUT/mini-TnS Cm x BB2000 This study BB2128 swr-2128::Tn5 Cm Swr- Mot- pUT/mini-TnS Cm x BB2000 This study BB2178 swr-2178::TnS Cm Swr- Che- pUT/mini-Tn5 Cm x BB2000 This study BB2180 swr-2180::Tn5 Cm Swrcr pUT/mini-Tn$ Cm x BB2000 This study BB2202 swr-2202::Tn5 Cm Swr Fla pUT/mini-Tn5 Cm x BB2000 This study a Che-, produces rotating flagella but defective in chemotactic response; Eloc, swarmer cell elongation constitutive; Elo-, lacking elongation of swarmer cell; Fla-, no 36.7-kDa flagellin produced; Mot-, produces nonrotating flagella; Swr-, absence of swarming on agar media; Swrcr, non-wild-type or crippled swarming and unusual consolidation patterns. b p. mirabilis mutants defective in swarmer cell differentiation and swarming motility. Produced from conjugal mating of E. coli harboring pUT/mini-TnS Cm and BB2000 (7). period of several hours and then stops (10, 12). This cessa- a secondary signal is evidently sensed when iron becomes tion of movement is accompanied by a dedifferentiation of limiting (28). The combination of conditions which inhibit the swarmer cell back to swimmer cell morphology, in a the rotation of the polar flagellum and limit the iron concen- process referred to as consolidation (see reference 37 for a tration is essential for initiation of transcription of the laf review). The cycle of swarming and consolidation is then genes (29). repeated several times until the agar surface is covered by Until recently (2), in-depth studies by modern techniques concentric rings formed by the swarming mass of bacteria have not been applied to understanding the genetic regula- (12). This cycle of events gives rise to the characteristic tion and sensory transduction mechanisms of swarmer cell bull's-eye appearance of P. mirabilis colonies (Fig. 1B). The differentiation and multicellular swarming of P. mirabilis. swarmer cell requires continuous contact with the surface to Since little is known about the genetic regulation of Proteus maintain the differentiated state. When removed from the swarming, we wanted a means of analysis which would be surface of an agar plate and suspended in liquid medium, independent of the mutant phenotype under investigation.
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