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Chapter 18 : Role of Cyclic Di-GMP in Biofilm Development and Signaling in

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Role of Cyclic Di-GMP in Biofilm Development and Signaling in , Page 1 of 2

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Abstract:

, a gram-negative bacterium and member of the family, is the causative agent of bubonic, septicemic, and pneumonic plague. In general, increased levels of cyclic di-GMP (c-di-GMP) inside bacterial cells correlate with biofilm formation and expression of exopolysaccharide (EPS) and adherence factors, while decreased intracellular levels stimulate motility and a planktonic lifestyle. c-di-GMP homeostasis is carried out by GGDEF domain proteins, cyclic diguanylate cyclases (DGCs), which synthesize c-di-GMP, as well as EAL and HD-GYP domain proteins, c-di-GMP phosphodiesterases (PDEs), which degrade this nucleotide. was reported to express an Hms-dependent biofilm EPS, based on electron microscopy, reaction with antisera against poly-β-1,6-GlcNAc, and on the ability of cells to bind Congo red (CR), calcofluor white, and ruthenium red, each shown to stain various polysaccharides. A mutant overproduces biofilm but shows no increase in the levels of HmsHFRS proteins. All other potential DGCs and PDEs encoded by the KIM6+ genome do not compensate for or mutations, and the authors' analysis suggests that HmsT and Y3730 are the only two functional DGCs and that HmsP is the only functional PDE in . Mutations in (encoding ornithine decarboxylase), (encoding arginine decarboxylase), or both genes cause progressively lower intracellular levels of putrescine and a corresponding loss of crystal violet staining as a measure of adherence. Currently, only biofilm development is known to be controlled by c-di-GMP signaling in .

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18

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Figures

Image of Figure 1.
Figure 1.

Transmission routes of plague. For simplicity, some occasional transmission routes are not shown. Transmission via ingestion of infected rodents by wild or domesticated carnivores and subsequent interaction with humans is not shown. This figure was slightly modified from a figure kindly provided by Ken Gage, CDC.

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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Image of Figure 2.
Figure 2.

Proposed model for life cycle regulation of by c-di-GMP. We hypothesize that c-di-GMP reciprocally regulates biofilm and virulence factors in High levels of c-di-GMP mediated by the GGDEF domain protein HmsT have been proven to be required for biofilm formation in the flea. During growth in mammals, decreases in c-di-GMP in cells due to the EAL domain protein HmsP lead to a transition to a planktonic state. We hypothesize that decreased c-di-GMP levels may also enhance expression of mammalian virulence factors. The image of the blocked flea was reproduced from Fig. 1B from Hinnebusch et al. ( ) with permission of the American Association for the Advancement of Science.

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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Image of Figure 3.
Figure 3.

Hms-dependent biofilm model of protein interactions and temperature regulation. Chains of circles represent linked monomers of the EPS component of the biofilm (different shades represent acetylated and deacetylated monomers). Predicted or hypothesized protein activities: HmsH, porin for polysaccharide export; HmsF, polysaccharide deacetylase; HmsR, glycosyl transferase; HmsS, assists HmsR in EPS synthesis. HmsT is a proven DGC (GGDEF domain), while HmsP is a proven c-di-GMP PDE (EAL domain). HmsP and HmsT form homodimers with HmsP interacting with HmsR and HmsT. HmsR also interacts with HmsS. HmsS is shown as a homodimer due to preliminary results that have not yet been confirmed. Cytoplasmic domains and periplasmic loops of IM proteins are shown as well as the putative lipoporotein linkage of HmsF and the periplasmic domain of HmsH. For simplicity, the defective GGDEF domain of HmsP is not shown. The plus sign indicates likely stimulation of HmsR enzymatic activity by c-di-GMP. At 26 to 34°C, Hms proteins are highly expressed (A), while at 37°C, the levels of Hms proteins are reduced to varying degrees (B). HmsT is degraded, thus reducing c-di-GMP levels. This, along with low levels of HmsR and HmsH, prevents significant biofilm formation. L-di-GMP, linear di-GMP; OM, outer membrane; GT, glycosyltransferase.

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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Image of Figure 4.
Figure 4.

Dot blot analysis of poly-β-1,6-GlcNAc-like EPS production by strains. cells were grown at 26°C overnight in PMH2 with 0.05% D-glucosamine, and crude polysaccharide extracts were spotted onto a nitrocellulose membrane. Blots were developed with antisera against purified polysaccharide intercellular adhesion of ( ).

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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Image of Figure 5.
Figure 5.

Confocal laser scanning microscopy images of green fluorescent protein-expressing cells. Cultures were grown at 26°C overnight in PMH2 with 0.2% glucose in a conical tube with a coverslip. Cells attached to the glass coverslip (at the air-liquid interface) were visualized with a Leica TCS laser scanning confocal microscope. The xzy plane (a cross-sectional view) is shown. Hms and HmsH strains are positive and negative controls, respectively. The figure uses black and white unpublished images from the experiment depicted in Fig. 6 from Kirillina et al. ( ).

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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Image of Figure 6.
Figure 6.

IM topology models of HmsP and HmsT. Dark grey boxes represent TM domains. Periplasmic and cytoplasmic domains are based on analysis of and fusions ( ). HAMP, EAL, and GGDEF domains are shown as light grey boxes. For HmsP, the GGDEF domain likely lacks DGC activity, since residues essential for this activity have been altered to SKTEF (shown in oval). E506 and D626 residues as well as the EAL motif within the EAL domain of HmsP are critical for PDE activity while the GGDEF residues of HmsT are essential for biofilm development ( ). Modified and reproduced from reference with permission of Blackwell Publishing.

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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Image of Figure 7.
Figure 7.

Western blot analysis of HmsR and HmsS protein levels in strains after growth at 26°Cor 37°C. Equal concentrations of whole-cell lysates were separated by sodium dodecyl sul-fate-polyacrylamide gel electrophoresis; immunoblots were reacted with antiserum against the indicated Hms proteins. The negative control lane has a whole-cell lysate from a mutant that lacks 102 kb of chromosomal DNA that includes the operon. Modified and reproduced from Kirillina et al. ( ) with permission of Blackwell Publishing.

Citation: Perry R, Bobrov A. 2010. Role of Cyclic Di-GMP in Biofilm Development and Signaling in , p 270-281. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch18
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