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Chapter 12 : The Scr Circuit in Modulates Swarming and Sticking

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Abstract:

The role of c-di-GMP in determining the switch between motile and sessile lifestyles appears to be an emerging theme in many bacteria; in some bacteria, one important consequence is an impact on virulence. Scr (swarming and capsular polysaccharide gene regulation) genes influence the lifestyle adaptation between swarming and sticking by modulating the cellular nucleotide pool. Fractionation experiments localize ScrA to the cytoplasm, ScrB in the periplasm, and ScrC with the cell membrane. Curiously, overproduction of ScrC without coproduction of ScrA and ScrB does not simply result in loss of increased expression but rather recapitulates the ScrABC phenotype. In contrast, both the GGDEF and the EAL domains of ScrC possess catalytic activity: by itself (in the absence of ScrA and ScrB), ScrC can synthesize c-di-GMP (in as well as in ), whereas in the context of functional ScrA and ScrB, ScrC is capable of degrading this secondary messenger. In comparison, the activity of ScrC seems to be modulated by ScrA and ScrB. The enzymes controlling the level of c-di-GMP include proteins with GGDEF and EAL domains as well as the phosphohydrolase-associated HD-GYP domain. In possessing a multiplicity of cell types appropriate for life under different circumstances, the swimmer, swarmer, and sticky cell types, the ubiquitous marine bacterium and human pathogen must make certain critical lifestyle determinations. c-di-GMP plays a key role by influencing this decision-making process.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12

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Gene Expression
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Figures

Image of Figure 1.
Figure 1.

Lifestyle decision for to swim, swarm, or stick? When growing in liquid, the highly motile swimmer cell is propelled by a single polar flagellum. Upon contact with surfaces, this polar flagellum is no longer an effective propulsive organelle. Unable to rotate its polar flagellum, the organism must decide whether to induce a second flagellar system and differentiate to the elongated, hyperflagellated swarmer cell or to orchestrate the production of sticky cell surface molecules promoting adhesion and biofilm development. This decision is modulated by Scr sensors that are thought to integrate environmental information by modulating the level of c-di-GMP. High levels of c-di-GMP promote the sessile lifestyle, whereas low levels of c-di-GMP enhance surface motility.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12
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Image of Figure 2.
Figure 2.

Swarming and sticking are reciprocally influenced at the level of transcription by the operon. Mutants with defects in the operon fail to swarm on solid surfaces (A) and produce crinkly colonies on Congo red medium (B). The inability of these mutants to swarm is not the simple consequence of being too sticky to move, as they also fail to swarm upon introduction of a lesion in the CPS biosynthetic locus (C). The altered phenotypes are a consequence of altered lateral flagellar () and gene expression. Transcription was measured in (D) and (E) reporter strains.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12
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Image of Figure 3.
Figure 3.

ScrC is a bifunctional enzyme whose activity is influenced by ScrA and ScrB. (A) Examination of P-labeled nucleotides extracted from a Δ strain carrying expression clones by using two-dimensional thin-layer chromatography (2D-TLC). The small arrows indicate control spots to provide orientation, and the large arrow indicates c-di-GMP. ScrABC decreases the c-di-GMP spot, the EAL domain is critical for the phosphodiesterase (PDE) activity of ScrABC, and ScrC produced by itself (without the context of functional ScrA and ScrB) increases the level of this nucleotide. (B) The EAL domain determines the PDE activity of ScrABC but not the diguanylate cyclase activity of ScrC: phenotypes of the wild-type (Wt) strain on swarm plates and Congo red medium upon ectopic expression of alleles.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12
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Image of Figure 4.
Figure 4.

ScrG is a second GGDEF-EAL protein participating in the control of swarming and sticking. (A) Although the phenotype is less profound than the phenotype on standard swarming agar, defects become apparent on low-salt swarming medium, which is less permissive for swarming than the standard high-salt swarming medium. The phenotype can be complemented by or but not by . (B) The effects of and are cumulative on swarming and colony morphology but not on swimming. Wild-type and mutant strains were inoculated in high-salt swarm plates (1.5% agar), high-salt, iron-supplemented (enhances colony rugosity) swarm plates (1.5% agar), Congo red medium (2% agar), and semisolid swim medium (0.3% agar). ScrG mutants (row 4) show slight impairment of swarming on high-salt agar; however, in combination with an deletion, the ability of the double mutant (row 3) to swarm is more defective than that of the single mutant strain (row 2). In addition, the colony morphology of the double mutant strain is more crinkly than either of the single mutant strains (shown on high-iron and Congo red media). The system has a negligible impact on swimming motility: all mutants show little difference in their ability to swim compared to the wild type.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12
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Image of Figure 5.
Figure 5.

Model of the Scr c-di-GMP circuit in transcriptional control of swarming and sticking. Two GGDEF-EAL proteins, ScrC and ScrG, regulate swarming and sticking gene expression by acting as phosphodiesterases to modulate the level of c-di-GMP. The phosphodiesterase activity of ScrC is controlled by interaction with ScrA, a predicted pyridoxal phosphate-dependent aminotransferase, and ScrB, a predicted periplasmic solute-binding protein. Potentially, input signals transmitted via the periplasmic sensing domain of ScrC and the PAS domain of ScrG may moderate the activity of the output GGDEF-EAL domains. High levels of c-di-GMP promote production of CPS production and biofilm formation, and low levels of this signaling molecule promote swarming motility. Additional output targets include a predicted cell surface adhesin binding chitin or -acetylglucosamine (VPA1598) and the operon, which encodes a type I membrane fusion transport system that is known to play a role in biofilm development (VPA1443-5). The nature of the input signals and how alterations in the cellular c-di-GMP pool affect transcription of lateral flagellar and genes are not known, although Cps-specific transcriptional regulators (CpsR and CpsS) participating in this circuit have been identified. This model also predicts the existence of additional GGDEF-, EAL-, or HD-GYP-type Scr sensors, and current work is focused on identifying new members of the Scr sensory array.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12
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Image of Figure 6.
Figure 6.

Additional output targets of the Scr circuit. c-di-GMP affects transcription of two known additional targets. Colonies containing bioluminescence () fusions were grown overnight on plates and photographed in the dark. All colonies grew equally well on the plate, but only the luminous colonies appear in the photograph. The luminescence of is enhanced by low levels of c-di-GMP (the consequence of overexpression of ) and repressed by high levels of c-di-GMP (upon overexpression of ) compared to strains carrying a vector control. In contrast, the fusion in is regulated oppositely, i.e., light production is enhanced by high levels of c-di-GMP and repressed by low levels of the nucleotide signal. Both genes encode predicted cell surface moieties. VPA1598 encodes a chitin- or -acetylglucosamine-binding protein. VPA1443 is in the operon, which encodes an RTX transporter system known to participate in biofilm development and affect colony morphology. Thus the Scr circuit, originally named for swarming and cps regulation, influences warming and ell surface egulation.

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12
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Tables

Generic image for table
Table 1

V. proteins with GGDEF, EAL, or HD domains

Citation: McCarter L. 2010. The Scr Circuit in Modulates Swarming and Sticking, p 173-185. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch12

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