Role of the Umo Proteins and the Rcs Phosphorelay in the Swarming Motility of the Wild Type and an O-Antigen (
            <i>waaL</i>
            ) Mutant of Proteus mirabilis

Morgenstein, Randy M.; Rather, Philip N.

doi:10.1128/jb.06047-11

Cited by 42 publications

(47 citation statements)

References 45 publications

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“…In support of our hypothesis, Morgenstein and Rather have suggested UmoB and UmoD are involved in activation of the Rcs system that acts to control swarming (26). Furthermore, we have shown that mutations in the Rcs system, specifically those in rcsC or rcsD (formerly rsbA), result in an Elo ϩ cells and precocious swarming (22) that partially phenocopy ⌬fliL cells.…”

Section: Discussionsupporting

confidence: 58%

“…qRT-PCR analysis showed that transcription of flhDC in broth-grown cells at 2.75 h (when YL1006 produces the maximum number of HPCs) is not different from that of the wild type (data not shown). Since the function of umo genes is thought to take part in flhDC expression, we measured the expression of umoB and umoD, which are also involved in swarming motility (26). As observed with umoA, umoD expression increased in ⌬fliL cells compared with wild-type cells, but by a smaller amount (1.1 to 1.5ϫ), while umoB expression remained unchanged (Table 3).…”

Section: Resultsmentioning

confidence: 99%

“…umoA, encoding a putative outer membrane protein, contains both 70 -dependent and 28 -dependent (flagellar class 3) promoters (25), hinting that umoA may be a novel member of the flagellar regulon. Morgenstein and Rather have suggested that UmoB and UmoD are in a pathway that activates the Rcs phosphorelay system (26). How the Umo proteins function to increase flhDC expression is unclear.…”

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Loss of FliL Alters Proteus mirabilis Surface Sensing and Temperature-Dependent Swarming

Lee

Belas

2015

J Bacteriol

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Proteus mirabilis is a dimorphic motile bacterium well known for its flagellum-dependent swarming motility over surfaces. In liquid, P. mirabilis cells are 1.5-to 2.0-m swimmer cells with 4 to 6 flagella. When P. mirabilis encounters a solid surface, where flagellar rotation is limited, swimmer cells differentiate into elongated (10-to 80-m), highly flagellated swarmer cells. In order for P. mirabilis to swarm, it first needs to detect a surface. The ubiquitous but functionally enigmatic flagellar basal body protein FliL is involved in P. mirabilis surface sensing. Previous studies have suggested that FliL is essential for swarming through its involvement in viscosity-dependent monitoring of flagellar rotation. In this study, we constructed and characterized ⌬fliL mutants of P. mirabilis and Escherichia coli. Unexpectedly and unlike other fliL mutants, both P. mirabilis and E. coli ⌬fliL cells swarm (Swr ؉ ). Further analysis revealed that P. mirabilis ⌬fliL cells also exhibit an alteration in their ability to sense a surface: e.g., ⌬fliL P. mirabilis cells swarm precociously over surfaces with low viscosity that normally impede wild-type swarming. Precocious swarming is due to an increase in the number of elongated swarmer cells in the population. Loss of fliL also results in an inhibition of swarming at <30°C. E. coli ⌬fliL cells also exhibit temperature-sensitive swarming. These results suggest an involvement of FliL in the energetics and function of the flagellar motor. Most bacteria are able to live a planktonic free-living lifestyle or in a surface-attached microbial community called a "biofilm." The interchange between the motile and the sessile phases, referred to as the "swim-or-stick" switch, is not merely stochastic. Rather, the lifestyle change occurs in response to cues that a cell senses as it nears a surface (1). These surface signals are required and initiate biofilm formation (1). A fundamental question underlying the transition in lifestyle from motile to sessile phases is how does a bacterium sense a surface?Studies of many different bacterial species support the idea that surface sensing often involves the bacterial flagellum (2), which also facilitates movement toward and attachment to a surface. However, it is generally agreed that motility and biofilm formation are mutually exclusive. Moreover, flagella are used not only for swimming in liquid but also for swarming over a solid surface. Many bacterial species swarm, and often, as in Proteus mirabilis, require a surface-induced differentiated cell type, called a swarmer cell, that is elongated and hyperflagellated (3).P. mirabilis is a Gram-negative gammaproteobacterium belonging to the Enterobacteriaceae family. It is an opportunistic pathogen capable of causing urinary tract infections (UTI) (4-6). P. mirabilis is dimorphic and produces short vegetative swimmer cells (1.5 to 2.0 m in length) with a single nucleoid and 4 to 10 peritrichous flagella when cultured in nutrient broth. Conversely, when cultured on nutrient agar or in viscous en...

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Section: Discussionsupporting

confidence: 58%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Loss of FliL Alters Proteus mirabilis Surface Sensing and Temperature-Dependent Swarming

Lee

Belas

2015

J Bacteriol

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“…Regulation of the swarm cell differentiation process is not fully understood, but many components have been investigated and recently reviewed (15-17). For instance, surface contact and the resulting inhibition of flagellar rotation are critical for swarm cell differentiation in most strains (18), and a combination of surface contact and changes in cell wall and lipopolysaccharide composition ultimately promote activity of the flagellar master regulator FlhD 2 C 2 and expression of the flagellar genes (18)(19)(20)(21)(22). Factors that impact temporal regulation of swarming, swarm speed, or overall swarm pattern have also been identified, such as putrescine and certain fatty acids (23, 24).…”

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confidence: 99%

Initiation of Swarming Motility by Proteus mirabilis Occurs in Response to Specific Cues Present in Urine and Requires Excess L-Glutamine

Armbruster

Hodges

Mobley

2013

Journal of Bacteriology

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Proteus mirabilis, a leading cause of catheter-associated urinary tract infection (CaUTI), differentiates into swarm cells that migrate across catheter surfaces and medium solidified with 1.5% agar. While many genes and nutrient requirements involved in the swarming process have been identified, few studies have addressed the signals that promote initiation of swarming following initial contact with a surface. In this study, we show that P. mirabilis CaUTI isolates initiate swarming in response to specific nutrients and environmental cues. Thirty-three compounds, including amino acids, polyamines, fatty acids, and tricarboxylic acid (TCA) cycle intermediates, were tested for the ability to promote swarming when added to normally nonpermissive media. L-Arginine, L-glutamine, DL-histidine, malate, and DL-ornithine promoted swarming on several types of media without enhancing swimming motility or growth rate. Testing of isogenic mutants revealed that swarming in response to the cues required putrescine biosynthesis and pathways involved in amino acid metabolism. Furthermore, excess glutamine was found to be a strict requirement for swarming on normal swarm agar in addition to being a swarming cue under normally nonpermissive conditions. We thus conclude that initiation of swarming occurs in response to specific cues and that manipulating concentrations of key nutrient cues can signal whether or not a particular environment is permissive for swarming. U rinary tract infection (UTI) is one of the most common hospital-associated infections, with an estimated 424,000 cases and 13,000 UTI-related deaths in U.S. hospitals in 2002 (1). In addition, placement of an indwelling catheter predisposes individuals to the development of catheter-associated UTI (CaUTI), the most common type of nosocomial infection (2, 3). CaUTI is generally thought to be caused by self-inoculation of the catheter (4). Once bacteria have colonized the catheter, motile species can rapidly traverse the catheter surface to reach the bladder and potentially establish a UTI.The dimorphic, motile, Gram-negative bacterium Proteus mirabilis is one of the leading causative agents of CaUTI, responsible for up to 44% of these infections (3, 5-7). P. mirabilis infections frequently develop into cystitis and pyelonephritis and can be further complicated by catheter encrustation and formation of urinary stones (8, 9). P. mirabilis has fascinated scientists for over 125 years for its ability to differentiate from short swimmer cells into elongated swarm cells that express hundreds to thousands of flagella (10). These swarm cells interact intimately with one another to form multicellular rafts (11-13). In the context of CaUTI, P. mirabilis utilizes this process of swarming to migrate along the catheter surface, gaining entry to the bladder and causing painful and sometimes serious complications (3,14).Swarming is distinct from swimming motility in that it refers to multicellular flagellum-mediated migration across a surface rather than movement in liquid medium or...

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“…In a Bacillus cereus transcriptome, several genes, including flagellar genes, were seen to be differentially regulated on swarm agar (15). In B. subtilis and Proteus mirabilis, the cell envelope has been implicated as a sensor of surface conditions (16,17). While details of the signaling pathway are unknown, involvement of a response regulator, DegU, in controlling flagellar gene expression in B. subtilis (18,19) has allowed parallels to be drawn between DegU and the response regulator RcsB in the Rcs signaling pathway, which communicates membrane stress to the genome and influences regulation of a large number of genes, including the flagellar regulon (16).…”

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confidence: 99%

More than Motility: Salmonella Flagella Contribute to Overriding Friction and Facilitating Colony Hydration during Swarming

Partridge

Harshey

2012

Journal of Bacteriology

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We show in this study that Salmonella cells, which do not upregulate flagellar gene expression during swarming, also do not increase flagellar numbers per m of cell length as determined by systematic counting of both flagellar filaments and hooks. Instead, doubling of the average length of a swarmer cell by suppression of cell division effectively doubles the number of flagella per cell. The highest agar concentration at which Salmonella cells swarmed increased from the normal 0.5% to 1%, either when flagella were overproduced or when expression of the FliL protein was enhanced in conjunction with stator proteins MotAB. We surmise that bacteria use the resulting increase in motor power to overcome the higher friction associated with harder agar. Higher flagellar numbers also suppress the swarming defect of mutants with changes in the chemotaxis pathway that were previously shown to be defective in hydrating their colonies. Here we show that the swarming defect of these mutants can also be suppressed by application of osmolytes to the surface of swarm agar. The "dry" colony morphology displayed by che mutants was also observed with other mutants that do not actively rotate their flagella. The flagellum/motor thus participates in two functions critical for swarming, enabling hydration and overriding surface friction. We consider some ideas for how the flagellum might help attract water to the agar surface, where there is no free water. Swarming bacteria may be divided into two categories: robust swarmers, which can navigate across a hard agar surface (1.5% agar and above), and temperate swarmers, which can swarm only on a softer agar surface (0.5 to 0.8% agar) (1-3). Robust swarmers include polarly flagellated bacteria, which induce peritrichous flagellation upon surface contact, such as Azospirillum, Rhodospirillum, and Vibrio species, as well as the peritrichously flagellated Proteus species (4-6). These bacteria display a hyperflagellated and hyperelongated swarm cell morphology, which is dramatically different from their broth-grown (swimming) counterparts. Transcriptome studies have shown a swarming-specific gene expression program in the robust swarmers (7-10). In polarly flagellated bacteria, frictional forces on the surface are surmised to slow flagellar rotation and signal altered gene expression (11,12), an observation solidified by experiments demonstrating a direct relationship between motor speed and lateral flagellar (laf) gene transcription (13). How motor speed might be sensed and transduced to activate laf expression is unknown. This phenomenon is apparently unique to polarly flagellated bacteria.Temperate swarmers include Escherichia coli and Bacillus, Pseudomonas, Rhizobium, Salmonella, Serratia, and Yersinia species. Among these, Bacillus subtilis displays increased flagellar numbers and cell length (14), but this morphology is not as dramatic as that seen in the robust swarmers. In a Bacillus cereus transcriptome, several genes, including flagellar genes, were seen to be differentially regulat...

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Role of the Umo Proteins and the Rcs Phosphorelay in the Swarming Motility of the Wild Type and an O-Antigen ( waaL ) Mutant of Proteus mirabilis

Cited by 42 publications

References 45 publications

Loss of FliL Alters Proteus mirabilis Surface Sensing and Temperature-Dependent Swarming

Loss of FliL Alters Proteus mirabilis Surface Sensing and Temperature-Dependent Swarming

Initiation of Swarming Motility by Proteus mirabilis Occurs in Response to Specific Cues Present in Urine and Requires Excess L-Glutamine

More than Motility: Salmonella Flagella Contribute to Overriding Friction and Facilitating Colony Hydration during Swarming

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