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4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis
Author:
Lotte Søgaard-Andersen1
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Affiliations:
1: Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Str., 35043 Marburg, Germany
Content Type: Monograph
Publication Year:
2008
Book DOI:
10.1128/9781555815677
Chapter DOI:
10.1128/9781555815677.ch4
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Abstract:
The intercellular C-signal has a fundamental role in fruiting body morphogenesis in Myxococcus xanthus. In this chapter, our current understanding of how the C-signal acts at the molecular level to induce and coordinate events that are separated in time and space is discussed. The first evidence for intercellular signals important for fruiting body formation came from the isolation of a collection of mutants that displayed nonautonomous developmental defects. Importantly, aggregation, sporulation, and C-signal-dependent gene expression were induced earlier than in wild-type cells, whereas the rippling stage was completely skipped. Random transposon mutagenesis followed by screening for mutants with deficiencies in C-signal-dependent responses, isolation of extragenic suppressors of a csgA insertion mutant, proteomics, and biochemical analyses have been instrumental in the identification of proteins in this pathway. Several regulatory mechanisms help to restrict the activity of the pathway to starving cells. First, starvation induces the stringent response, which, in turn, induces csgA transcription and A-signal accumulation, which induces fruA transcription. Secondly, starvation induces mrpAB expression, and MrpAB induces mrpC transcription. Thirdly, by an unknown mechanism secretion of MXAN0206, the protease likely to cleave p25, is induced. Moreover, the establishment of cell-biology-based methods with green fluorescent protein (GFP) fusion proteins and immunofluorescence are likely to result in the detailed understanding of the spatial organization of M. xanthus cells during starvation.
Citation:
Søgaard-Andersen L.
2008.
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis,
p 77-91.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch4
Key Concept Ranking
- Type IV Pili
- 0.4594519
- Outer Membrane Proteins
- 0.41508508
- Gene Expression
- 0.40337256
0.4594519
Figures
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis
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Citation:
Søgaard-Andersen L.
2008.
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis,
p 77-91.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch4
/content/10.1128/9781555815677.ch04.ch04fig01
Figure 1
Schematic outline of fruiting body morphogenesis in M. xanthus. The different morphological stages are indicated. Triangles indicate genes that are induced at different time points during fruiting body formation. Filled and open triangles indicate C-signal-independent and -dependent genes, respectively. The times at which the intercellular A- and C-signals become important for development are indicated. The level of C-signaling that individual cells are exposed to is indicated by the level of gray. The grayscale below the timeline indicates C-signaling levels in individual cells.
10.1128/9781555815677/f0078-01_thmb.gif
10.1128/9781555815677/f0078-01.gif
Figure 1
Schematic outline of fruiting body morphogenesis in M. xanthus. The different morphological stages are indicated. Triangles indicate genes that are induced at different time points during fruiting body formation. Filled and open triangles indicate C-signal-independent and -dependent genes, respectively. The times at which the intercellular A- and C-signals become important for development are indicated. The level of C-signaling that individual cells are exposed to is indicated by the level of gray. The grayscale below the timeline indicates C-signaling levels in individual cells.
Citation:
Søgaard-Andersen L.
2008.
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis,
p 77-91.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch4
/content/10.1128/9781555815677.ch04.ch04fig02
Figure 2
The C-signal transduction pathway. (A) Model of the C-signal transduction pathway. Three different levels of phosphorylated FruA (FruA-P) are indicated, with the stippled circle indicating a low level and the heavy circle indicating a high level of phosphorylation. The encircled numbers indicate processes initiated at low, intermediate, and high levels of C-signaling and which may correspond to low, intermediate, and high levels of FruA phosphorylation, respectively. The shaded box indicates the site of convergence of the MXAN4899, SdeK, TodK, and RodK pathways with the C-signal transduction pathway. See the text for details. (B) Regulation of MrpC activity. See the text for details.
10.1128/9781555815677/f0082-01_thmb.gif
10.1128/9781555815677/f0082-01.gif
Figure 2
The C-signal transduction pathway. (A) Model of the C-signal transduction pathway. Three different levels of phosphorylated FruA (FruA-P) are indicated, with the stippled circle indicating a low level and the heavy circle indicating a high level of phosphorylation. The encircled numbers indicate processes initiated at low, intermediate, and high levels of C-signaling and which may correspond to low, intermediate, and high levels of FruA phosphorylation, respectively. The shaded box indicates the site of convergence of the MXAN4899, SdeK, TodK, and RodK pathways with the C-signal transduction pathway. See the text for details. (B) Regulation of MrpC activity. See the text for details.
Citation:
Søgaard-Andersen L.
2008.
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis,
p 77-91.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch4
/content/10.1128/9781555815677.ch04.ch04fig03
Figure 3
A quantitative model for C-signal-induced responses. The three signal amplification loops in the C-signal transduction pathway are indicated. See the text for details.
10.1128/9781555815677/f0085-01_thmb.gif
10.1128/9781555815677/f0085-01.gif
Figure 3
A quantitative model for C-signal-induced responses. The three signal amplification loops in the C-signal transduction pathway are indicated. See the text for details.
Citation:
Søgaard-Andersen L.
2008.
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis,
p 77-91.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch4
/content/10.1128/9781555815677.ch04.ch04fig04
Figure 4
Model for C-signal-induced aggregation. (A) The basic event with the end-to-end contact between two cells with C-signal transmission followed by a change in cell behavior. (B) Chain formation. This event is a consequence of end-to-end contacts with C-signal transmission between. The formation of a chain depends on the sequential recruitment of cells as shown in the four panels. Cells engaged in C-signal transmission are shown to move towards an aggregation center indicated in gray to the left with a low reversal frequency. Non-C-signaling cells move with a high reversal frequency as indicated by the double-headed arrow. (C) Stream formation. Movement of cells in a chain is predicted to create alignment of neighboring cells with the formation of secondary chains of cells (marked by dark color). Cells in secondary chains are associated with the primary chain by lateral cell-cell contacts and with other cells in the secondary chain by end-to-end contacts. Together, an initiating chain and its associated secondary chains will make up a stream. (D) Stream formation in vivo. Cell arrangements were visualized by fluorescence microscopy of GFP-labeled cells. GFP-labeled wild-type cells were codeveloped with nonfluorescent wild-type cells at a ratio of 1 to 40. Images were acquired after the indicated hours of starvation. Circles in the 6-h image indicate aggregation centers; arrows indicate streams. Scale bar, 50 μm.
10.1128/9781555815677/f0088-01_thmb.gif
10.1128/9781555815677/f0088-01.gif
Figure 4
Model for C-signal-induced aggregation. (A) The basic event with the end-to-end contact between two cells with C-signal transmission followed by a change in cell behavior. (B) Chain formation. This event is a consequence of end-to-end contacts with C-signal transmission between. The formation of a chain depends on the sequential recruitment of cells as shown in the four panels. Cells engaged in C-signal transmission are shown to move towards an aggregation center indicated in gray to the left with a low reversal frequency. Non-C-signaling cells move with a high reversal frequency as indicated by the double-headed arrow. (C) Stream formation. Movement of cells in a chain is predicted to create alignment of neighboring cells with the formation of secondary chains of cells (marked by dark color). Cells in secondary chains are associated with the primary chain by lateral cell-cell contacts and with other cells in the secondary chain by end-to-end contacts. Together, an initiating chain and its associated secondary chains will make up a stream. (D) Stream formation in vivo. Cell arrangements were visualized by fluorescence microscopy of GFP-labeled cells. GFP-labeled wild-type cells were codeveloped with nonfluorescent wild-type cells at a ratio of 1 to 40. Images were acquired after the indicated hours of starvation. Circles in the 6-h image indicate aggregation centers; arrows indicate streams. Scale bar, 50 μm.
Citation:
Søgaard-Andersen L.
2008.
4 Contact-Dependent Signaling in Myxococcus xanthus : the Function of the C-Signal in Fruiting Body Morphogenesis,
p 77-91.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch4
References
/content/book/10.1128/9781555815677.ch04
1.
Baker, M. E. 1994. Myxococcus xanthus C-factor, a morphogenetic paracrine signal, is similar to Escherichia coli3-oxoacyl-[acyl-carrier-protein] reductase and human 17 beta-hydroxysteroid dehydrogenase. Biochem. J. 301: 311– 312.
2.
Blackhart, B. D., and, D. R. Zusman. 1985. “Frizzy” genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc. Natl. Acad. Sci. USA 82: 8771– 8774.
3.
Boysen, A.,, E. Ellehauge,, B. Julien, and, L. Søgaard-Andersen. 2002. The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 184: 1540– 1546.
4.
Cho, K., and, D. R. Zusman. 1999. Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol. Microbiol. 34: 714– 725.
5.
Crawford, E. W., and, L. J. Shimkets. 2000. The Myxococcus xanthus socE and csgA genes are regulated by the stringent response. Mol. Microbiol. 37: 788– 799.
6.
Cusick, J. K.,, E. Hager, and, R. E. Gill. 2002. Characterization of bcsA mutations that bypass two distinct signaling requirements for Myxococcus xanthus development. J. Bacteriol. 184: 5141– 5150.
7.
Diodati, M. E.,, F. Ossa,, N. B. Caberoy,, I. R. Jose,, W. Hiraiwa,, M. M. Igo,, M. Singer, and, A. G. Garza. 2006. Nla18, a key regulatory protein required for normal growth and development of Myxococcus xanthus. J. Bacteriol. 188: 1733– 1743.
8.
Downard, J.,, S. V. Ramaswamy, and, K. S. Kil. 1993. Identification of esg, a genetic locus involved in cell-cell signaling during Myxococcus xanthus development. J. Bacteriol. 175: 7762– 7770.
9.
Ellehauge, E.,, M. Nørregaard-Madsen, and, L. Søgaard-Andersen. 1998. The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in M. xanthus development. Mol. Microbiol. 30: 807– 817.
10.
Garza, A. G.,, J. S. Pollack,, B. Z. Harris,, A. Lee,, I. M. Keseler,, E. F. Licking, and, M. Singer. 1998. SdeK is required for early fruiting body development in Myxococcus xanthus. J. Bacteriol. 180: 4628– 4637.
11.
Gronewold, T. M. A., and, D. Kaiser. 2001. The act operon controls the level and time of C-signal production for Myxococcus xanthus development. Mol. Microbiol. 40: 744– 756.
12.
Guo, D.,, M. G. Bowden,, R. Pershad, and, H. B. Kaplan. 1996. The Myxococcus xanthus rfbABC operon encodes an ATP-binding cassette transporter homolog required for O-antigen biosynthesis and multicellular development. J. Bacteriol. 178: 1631– 1639.
13.
Hagen, D. C.,, A. P. Bretscher, and, D. Kaiser. 1978. Synergism between morphogenetic mutants of Myxococcus xanthus. Dev. Biol. 64: 284– 296.
14.
Hager, E.,, H. Tse, and, R. E. Gill. 2001. Identification and characterization of spdR mutations that bypass the BsgA protease-dependent regulation of developmental gene expression in Myxococcus xanthus. Mol. Microbiol. 39: 765– 780.
15.
Harris, B. Z.,, D. Kaiser, and, M. Singer. 1998. The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes Dev. 12: 1022– 1035.
16.
Hodgkin, J., and, D. Kaiser. 1979. Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol. Gen. Genet. 171: 177– 191.
17.
Horiuchi, T.,, T. Akiyama,, S. Inouye, and, T. Komano. 2002a. Analysis of dofA, a fruA-dependent developmental gene, and its homologue, dofB, in Myxococcus xanthus. J. Bacteriol. 184: 6803– 6810.
18.
Horiuchi, T.,, M. Taoka,, T. Isobe,, T. Komano, and, S. Inouye. 2002b. Role of fruA and csgA genes in gene expression during development of Myxococcus xanthus. Analysis by two-dimensional gel electrophoresis. J. Biol. Chem. 277: 26753– 26760.
19.
Inouye, M.,, S. Inouye, and, D. R. Zusman. 1979a. Gene expression during development of Myxococcus xanthus: pattern of protein synthesis. Dev. Biol. 68: 579– 591.
20.
Inouye, M.,, S. Inouye, and, D. R. Zusman. 1979b. Biosynthesis and self-assembly of protein S, a development specifc protein of Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 76: 209– 213.
21.
Jelsbak, L., and, L. Søgaard-Andersen. 1999. The cell surface-associated intercellular C-signal induces behavioral changes in individual Myxococcus xanthus cells during fruiting body morphogenesis. Proc. Natl. Acad. Sci. USA 96: 5031– 5036.
22.
Jelsbak, L., and, L. Søgaard-Andersen. 2002. Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 99: 2032– 2037.
23.
Jelsbak, L.,, M. Givskov, and, D. Kaiser. 2005. Enhancer-binding proteins with a forkhead-associated domain and the sigma54 regulon in Myxococcus xanthus fruiting body development. Proc. Natl. Acad. Sci. USA 102: 3010– 3015.
24.
Jenal, U. 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol. 7: 185– 191.
25.
Julien, B.,, A. D. Kaiser, and, A. Garza. 2000. Spatial control of cell differentiation in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 97: 9098– 9103.
26.
Kaiser, D. 1979. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 76: 5952– 5956.
27.
Kaiser, D. 2003. Coupling cell movement to multicellular development in myxobacteria. Nat. Rev. Microbiol. 1: 45– 54.
28.
Kim, S. K., and, D. Kaiser. 1990a. Cell alignment required in differentiation of Myxococcus xanthus. Science 249: 926– 928.
29.
Kim, S. K., and, D. Kaiser. 1990b. Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus. Genes Dev. 4: 896– 904.
30.
Kim, S. K., and, D. Kaiser. 1990c. Purification and properties of Myxococcus xanthus C-factor, an intercellular signaling protein. Proc. Natl. Acad. Sci. USA 87: 3635– 3639.
31.
Kim, S. K., and, D. Kaiser. 1990d. C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell 61: 19– 26.
32.
Kim, S. K., and, D. Kaiser. 1991. C-factor has distinct aggregation and sporulation thresholds during Myxococcus development. J. Bacteriol. 173: 1722– 1728.
33.
Kirby, J. R., and, D. R. Zusman. 2003. Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 100: 2008– 2013.
34.
Kroos, L.,, A. Kuspa, and, D. Kaiser. 1986. A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev. Biol. 117: 252– 266.
35.
Kroos, L., and, D. Kaiser. 1987. Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes Dev. 1: 840– 854.
36.
Kroos, L.,, P. Hartzell,, K. Stephens, and, D. Kaiser. 1988. A link between cell movement and gene expression argues that motility is required for cell-cell signaling during fruiting body development. Genes Dev. 2: 1677– 1685.
37.
Kruse, T.,, S. Lobedanz,, N. M. S. Berthelsen, and, L. Søgaard-Andersen. 2001. C-signal: a cell surface-associated morphogen that induces and coordinates multicellular fruiting body morphogenesis and sporulation in M. xanthus. Mol. Microbiol. 40: 156– 168.
38.
Kuspa, A.,, L. Kroos, and, D. Kaiser. 1986. Intercellular signaling is required for developmental gene expression in Myxococcus xanthus. Dev. Biol. 117: 267– 276.
39.
Kuspa, A.,, L. Plamann, and, D. Kaiser. 1992a. A-signalling and the cell density requirement for Myxococcus xanthus development. J. Bacteriol. 174: 7360– 7369.
40.
Kuspa, A.,, L. Plamann, and, D. Kaiser. 1992b. Identification of heat-stable A-factor from Myxococcus xanthus. J. Bacteriol. 174: 3319– 3326.
41.
Lee, B.-U.,, K. Lee,, J. Mendez, and, L. J. Shimkets. 1995. A tactile sensory system of Myxococcus xanthus involves an extracellular NAD(P) +-containing protein. Genes Dev. 9: 2964– 2973.
42.
Lee, K., and, L. J. Shimkets. 1994. Cloning and characterization of the socA locus which restores development to Myxococcus xanthus C-signaling mutants. J. Bacteriol. 176: 2200– 2209.
43.
Lee, K., and, L. J. Shimkets. 1996. Suppression of a signaling defect during Myxococcus xanthus development. J. Bacteriol. 178: 977– 984.
44.
Li, J.,, G. I. Lee,, S. R. Van Doren, and, J. C. Walker. 2000. The FHA domain mediates phosphoprotein interactions. J. Cell Sci. 113: 4143– 4149.
45.
Li, S.,, B.-U. Lee, and, L. J. Shimkets. 1992. csgA expression entrains Myxococcus xanthus development. Genes Dev. 6: 401– 410.
46.
Licking, E.,, L. Gorski, and, D. Kaiser. 2000. A common step for changing cell shape in fruiting body and starvation-independent sporulation in Myxococcus xanthus. J. Bacteriol. 182: 3553– 3558.
47.
Lobedanz, S., and, L. Søgaard-Andersen. 2003. Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev. 17: 2151– 2161.
48.
McBride, M. J.,, R. A. Weinberg, and, D. R. Zusman. 1989. “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc. Natl. Acad. Sci. USA 86: 424– 428.
49.
McBride, M. J.,, T. Köhler, and, D. R. Zusman. 1992. Methylation of FrzCD, a methyl-accepting taxis protein of Myxococcus xanthus, is correlated with factors affecting cell behavior. J. Bacteriol. 174: 4246– 4257.
50.
Merz, A. J.,, M. So, and, M. P. Sheetz. 2000. Pilus retraction powers bacterial twitching motility. Nature 407: 98– 102.
51.
Mignot, T.,, J. P. Merlie, and, D. R. Zusman. 2005. Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310: 855– 857.
52.
Mignot, T.,, J. W. Shaevitz,, P. L. Hartzell, and, D. R. Zusman. 2007. Evidence that focal adhesion complexes power bacterial gliding motility. Science 315: 853– 856.
53.
Munoz, D. J.,, S. Inouye, and, M. Inouye. 1991. A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a gram-negative bacterium. Cell 67: 995– 1006.
54.
Nariya, H., and, S. Inouye. 2005. Identification of a protein Ser/Thr kinase cascade that regulates essential transcriptional activators in Myxococcus xanthus development. Mol. Microbiol. 58: 367– 379.
55.
Nariya, H., and, S. Inouye. 2006. A protein Ser/Thr kinase cascade negatively regulates the DNA-binding activity of MrpC, a smaller form of which may be necessary for the Myxococcus xanthus development. Mol. Microbiol. 60: 1205– 1217.
56.
O’Connor, K. A., and, D. R. Zusman. 1989. Patterns of cellular interactions during fruiting-body formation in Myxococcus xanthus. J. Bacteriol. 171: 6013– 6024.
57.
O’Connor, K. A., and, D. R. Zusman. 1991. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J. Bacteriol. 173: 3318– 3333.
58.
Ogawa, M.,, S. Fujitani,, X. Mao,, S. Inouye, and, T. Komano. 1996. FruA, a putative transcription factor essential for the development of Myxococus xanthus. Mol. Microbiol. 22: 757– 767.
59.
Oppermann, U.,, C. Filling,, M. Hult,, N. Shafqat,, X. Wu,, M. Lindh,, J. Shafqat,, E. Nordling,, Y. Kallberg,, B. Persson, and, H. Jornvall. 2003. Short-chain dehydrogenases/reductases (SDR): the 2002 update. Chem. Biol. Interact. 143–144: 247– 253.
60.
Overgaard, M.,, S. Wegener-Feldbrügge, and, L. Søgaard-Ander-sen. 2006. The orphan response regulator DigR is required for synthesis of extracellular matrix fibrils in Myxococcus xanthus. J. Bacteriol. 188: 4384– 4394.
61.
Plamann, L.,, A. Kuspa, and, D. Kaiser. 1992. Proteins that rescue A-signal-defective mutants of Myxococcus xanthus. J. Bacteriol. 174: 3311– 3318.
62.
Pollack, J. S., and, M. Singer. 2001. SdeK, a histidine kinase required for Myxococcus xanthus development. J. Bacteriol. 183: 3589– 3596.
63.
Rasmussen, A. A., and, L. Søgaard-Andersen. 2003. TodK, a putative histidine protein kinase, regulates timing of fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 185: 5452– 5464.
64.
Rasmussen, A. A.,, S. L. Porter,, J. P. Armitage, and, L. Søgaard-Andersen. 2005. Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase during fruiting body morphogenesis in Myxococcus xanthus. Mol. Microbiol. 56: 1358– 1372.
65.
Rasmussen, A. A.,, S. Wegener-Feldbrügge,, S. L. Porter,, J. P. Armitage, and, L. Søgaard-Andersen. 2006. Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Mol. Microbiol. 60: 525– 534.
66.
Reichenbach, H. 1965. Rhythmische vorgänge bei der Schwarmenfaltung von Myxobakterien. Ber. Dtsch. Bot. Ges. 78: 102– 105.
67.
Reichenbach, H. 1999. The ecology of the myxobacteria. Environ. Microbiol. 1: 15– 21.
68.
Rosenbluh, A.,, R. Nir,, E. Sahar, and, E. Rosenberg. 1989. Cell-density-dependent lysis and sporulation of Myxococcus xanthus in agarose beads. J. Bacteriol. 171: 4923– 4929.
69.
Sager, B., and, D. Kaiser. 1994. Intercellular C-signaling and the traveling waves of Myxococcus. Genes Dev. 8: 2793– 2804.
70.
Shimkets, L. J., and, D. Kaiser. 1982. Induction of coordinated movement of Myxococcus xanthus cells. J. Bacteriol. 152: 451– 461.
71.
Shimkets, L. J.,, R. E. Gill, and, D. Kaiser. 1983. Developmental cell interactions in Myxococcus xanthus and the spoC locus. Proc. Natl. Acad. Sci. USA 80: 1406– 1410.
72.
Shimkets, L. J., and, H. Rafiee. 1990. CsgA, an extracellular protein essential for Myxococcus xanthus development. J. Bacteriol. 172: 5299– 5306.
73.
Singer, M., and, D. Kaiser. 1995. Ectopic production of guanosine penta- and tetraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Genes Dev. 9: 1633– 1644.
74.
Skerker, J. M., and, H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98: 6901– 6904.
75.
Søgaard-Andersen, L., and, D. Kaiser. 1996. C factor, a cell-surface-associated intercellular signaling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 93: 2675– 2679.
76.
Søgaard-Andersen, L.,, F. J. Slack,, H. Kimsey, and, D. Kaiser. 1996. Intercellular C-signaling in Myxococcus xanthus involves a branched signal transduction pathway. Genes Dev. 10: 740– 754.
77.
Søgaard-Andersen, L.,, M. Overgaard,, S. Lobedanz,, E. Ellehauge,, L. Jelsbak, and, A. A. Rasmussen. 2003. Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus. Mol. Microbiol. 48: 1– 8.
78.
Søgaard-Andersen, L. 2004. Cell polarity, intercellular signalling and morphogenetic cell movements in Myxococcus xanthus. Curr. Opin. Microbiol. 7: 587– 593.
79.
Spormann, A. M., and, A. D. Kaiser. 1995. Gliding movements in Myxococcus xanthus. J. Bacteriol. 177: 5846– 5852.
80.
Sun, H.,, D. R. Zusman, and, W. Shi. 2000. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10: 1143– 1146.
81.
Sun, H., and, W. Shi. 2001a. Genetic studies of mrp, a locus essential for cellular aggregation and sporulation of Myxococcus xanthus. J. Bacteriol. 183: 4786– 4795.
82.
Sun, H., and, W. Shi. 2001b. Analyses of mrp genes during Myxococcus xanthus development. J. Bacteriol. 183: 6733– 6739.
83.
Taylor, B. L., and, I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63: 479– 506.
84.
Udo, H.,, M. Inouye, and, S. Inouye. 1996. Effects of overexpression of Pkn2, a transmembrane protein serine/ threonine kinase, on development of Myxococcus xanthus. J. Bacteriol. 178: 6647– 6649.
85.
Ueki, T., and, S. Inouye. 2003. Identification of an activator protein required for the induction of fruA, a gene essential for fruiting body development in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 100: 8782– 8787.
86.
Ueki, T., and, S. Inouye. 2005a. Identification of a gene involved in polysaccharide export as a transcription target of FruA, an essential factor for Myxococcus xanthus development. J. Biol. Chem. 280: 32279– 32284.
87.
Ueki, T., and, S. Inouye. 2005b. Activation of a development-specific gene, dofA, by FruA, an essential transcription factor for development of Myxococcus xanthus. J. Bacteriol. 187: 8504– 8506.
88.
Ward, M. J., and, D. R. Zusman. 1999. Motility in Myxococcus xanthus and its role in developmental aggregation. Curr. Opin. Microbiol. 2: 624– 629.
89.
Welch, R., and, D. Kaiser. 2001. Pattern formation and traveling waves in myxobacteria: experimental demonstration. Proc. Natl. Acad. Sci. USA 98: 14907– 14912.
90.
Wolgemuth, C.,, E. Hoiczyk,, D. Kaiser, and, G. Oster. 2002. How myxobacteria glide. Curr. Biol. 12: 369– 377.
91.
Wu, S. S., and, D. Kaiser. 1995. Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol. Microbiol. 18: 547– 558.
92.
Yoder-Himes, D. R., and, L. Kroos. 2006. Regulation of the Myxococcus xanthus C-signal-dependent omega4400 promoter by the essential developmental protein FruA. J. Bacteriol. 188: 5167– 5176.