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12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network
Authors:
Montserrat Elías-Arnanz1,
Marta Fontes2,
S. Padmanabhan3
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Affiliations:
1: Departamento de Genética y Microbiología, Facultad de Biología, Universidad de Murcia, 30100 Murcia, Spain;
2: Departamento de Genética y Microbiología, Facultad de Biología, Universidad de Murcia, 30100 Murcia, Spain;
3: Departamento de Genética y Microbiología, Facultad de Biología, Universidad de Murcia, 30100 Murcia, Spain
Content Type: Monograph
Publication Year:
2008
Book DOI:
10.1128/9781555815677
Chapter DOI:
10.1128/9781555815677.ch12
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Abstract:
Myxobacteria frequently occur as brightly colored colonies and sporangioles, due to the presence of carotenoids and/or other pigments. This chapter provides an update on the considerable amount of new information that has since been acquired with respect to the inducing signals, their reception and transduction, and the transcriptional regulation of the structural genes involved in carotenoid biosynthesis in Myxococcus xanthus. The observation that the action spectra for photolysis and carotenogenesis in M. xanthus were similar and corresponded closely to the absorption spectrum of the iron-containing protoporphyrin IX, led to the proposal that this compound was the photosensitizer that linked the processes of photolysis and carotenogenesis. The carD gene was identified in a screen for Car- mutants among a large collection of strains bearing Tn5 insertions. Recent studies have identified a new factor, CarG (the product of the gene directly downstream of carD), which is required in every CarD-dependent process analyzed. The CarA operator design and the mechanism underlying the repression-antirepression switch of PB have been subjected to detailed molecular analysis. The most studied phenomenon in M. xanthus is undoubtedly its striking ability to form multicellular fruiting bodies on starvation, a process that has served as a prokaryotic model for the study of cell-cell interactions and cellular differentiation. Studies with M. xanthus continue to provide insights into the general principles underlying the complexity of the biosynthetic pathways and regulatory mechanisms involved in eubacterial carotenogenesis.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
Figures
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network
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Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
/content/10.1128/9781555815677.ch12.ch12fig01
Figure 1
Known genetic elements involved in carotenogenesis and their interactions. Squat arrows show photoinducible genes (crtIb) or operons (carQRS and the carB-carA cluster with the constituent genes indicated) implicated in the carotenogenic pathway. Genes for other proteins involved whose expression is not light dependent are not shown. Labeled ovals are the regulatory factors that have been identified and characterized, with continuous arrows indicating positive regulation, and blunt-ended lines indicating negative regulation. Carotenoid biosynthesis enzymes are encoded by crtIb, all of the genes in the carB operon, and crtYc and crtYd in the carA operon. The latter operon also codes for the regulatory factors CarA and Orf11. See the text for further explanation.
10.1128/9781555815677/f0213-01_thmb.gif
10.1128/9781555815677/f0213-01.gif
Figure 1
Known genetic elements involved in carotenogenesis and their interactions. Squat arrows show photoinducible genes (crtIb) or operons (carQRS and the carB-carA cluster with the constituent genes indicated) implicated in the carotenogenic pathway. Genes for other proteins involved whose expression is not light dependent are not shown. Labeled ovals are the regulatory factors that have been identified and characterized, with continuous arrows indicating positive regulation, and blunt-ended lines indicating negative regulation. Carotenoid biosynthesis enzymes are encoded by crtIb, all of the genes in the carB operon, and crtYc and crtYd in the carA operon. The latter operon also codes for the regulatory factors CarA and Orf11. See the text for further explanation.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
/content/10.1128/9781555815677.ch12.ch12fig02
Figure 2
Carotenoid biosynthetic pathway and the genes involved in each step. The proposed pathway for the biosynthesis of myxobacton, the primary carotenoid in M. xanthus, is shown. The roles of Orf6 and Orf9 remain to be defined but may be linked to the glycosyl- and acyltransferase activities, respectively, that are essential for production of myxobacton.
10.1128/9781555815677/f0214-01_thmb.gif
10.1128/9781555815677/f0214-01.gif
Figure 2
Carotenoid biosynthetic pathway and the genes involved in each step. The proposed pathway for the biosynthesis of myxobacton, the primary carotenoid in M. xanthus, is shown. The roles of Orf6 and Orf9 remain to be defined but may be linked to the glycosyl- and acyltransferase activities, respectively, that are essential for production of myxobacton.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
/content/10.1128/9781555815677.ch12.ch12fig03
Figure 3
Design of the light-inducible promoters identified in M. xanthus. Sequences show the promoter regions of PQRS, PI, and PB, the three M. xanthus light-inducible promoters. The –10 and –35 bases are marked for all three promoters. In PQRS, the CarD-binding site is boxed (with the two AT-rich tracts underlined). Two bases at the –35 region of PQRS, which on mutation remove light-induced promoter activity, are underlined (Whitworth et al., 2004). The bases underlined in the PI promoter sequence are critical for promoter activity (
Martínez-Argudo et al., 1998
). In the PB promoter region, the inverted repeats of the bipartite CarA operator, pI and pII, are boxed and marked by arrows.
10.1128/9781555815677/f0216-01_thmb.gif
10.1128/9781555815677/f0216-01.gif
Figure 3
Design of the light-inducible promoters identified in M. xanthus. Sequences show the promoter regions of PQRS, PI, and PB, the three M. xanthus light-inducible promoters. The –10 and –35 bases are marked for all three promoters. In PQRS, the CarD-binding site is boxed (with the two AT-rich tracts underlined). Two bases at the –35 region of PQRS, which on mutation remove light-induced promoter activity, are underlined (Whitworth et al., 2004). The bases underlined in the PI promoter sequence are critical for promoter activity ( Martínez-Argudo et al., 1998 ). In the PB promoter region, the inverted repeats of the bipartite CarA operator, pI and pII, are boxed and marked by arrows.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
/content/10.1128/9781555815677.ch12.ch12fig04
Figure 4
Domain organization of CarD. The independent domain formed by the first 180 N-terminal residues of CarD, which defines the family Pfam 02559 of CarD-like proteins, is schematically represented by an unfilled rectangle. The C-terminal HMGA-like domain is made up of two stretches: a highly acidic one represented by the filled rectangle (residues 183 to 228) and a basic one which contains the four AT-hook repeats represented by the four stippled boxes (residues 229 to 316). The specific CarD domains that interact with CarG and DNA are as indicated.
10.1128/9781555815677/f0217-01_thmb.gif
10.1128/9781555815677/f0217-01.gif
Figure 4
Domain organization of CarD. The independent domain formed by the first 180 N-terminal residues of CarD, which defines the family Pfam 02559 of CarD-like proteins, is schematically represented by an unfilled rectangle. The C-terminal HMGA-like domain is made up of two stretches: a highly acidic one represented by the filled rectangle (residues 183 to 228) and a basic one which contains the four AT-hook repeats represented by the four stippled boxes (residues 229 to 316). The specific CarD domains that interact with CarG and DNA are as indicated.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
/content/10.1128/9781555815677.ch12.ch12fig05
Figure 5
Model for the action of CarA and CarS in the regulation of the PB promoter. The dimeric CarA repressor is shown with its N- and C-terminal domains represented by the small and large spheres, respectively. In the dark (left panel), two CarA dimers bind via their N-terminal domains and in a cooperative fashion to the bipartite CarA operator. The two sites in the operator, palindromes pI and pII, are each shown as a pair of convergent arrows. Occupancy of pII by CarA blocks promoter access to the RNA polymerase holoenzyme (shown by the object labeled RNAP) leading to repression of carB. On exposure to light (right panel) CarS, shown by the dark ellipsoids, is produced, and its interaction with the N-terminal domain of CarA readily dismantles CarA-pII complexes. The RNA polymerase holoenzyme thereby gains access to the promoter, leading to the derepression of carB.
10.1128/9781555815677/f0220-01_thmb.gif
10.1128/9781555815677/f0220-01.gif
Figure 5
Model for the action of CarA and CarS in the regulation of the PB promoter. The dimeric CarA repressor is shown with its N- and C-terminal domains represented by the small and large spheres, respectively. In the dark (left panel), two CarA dimers bind via their N-terminal domains and in a cooperative fashion to the bipartite CarA operator. The two sites in the operator, palindromes pI and pII, are each shown as a pair of convergent arrows. Occupancy of pII by CarA blocks promoter access to the RNA polymerase holoenzyme (shown by the object labeled RNAP) leading to repression of carB. On exposure to light (right panel) CarS, shown by the dark ellipsoids, is produced, and its interaction with the N-terminal domain of CarA readily dismantles CarA-pII complexes. The RNA polymerase holoenzyme thereby gains access to the promoter, leading to the derepression of carB.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
/content/10.1128/9781555815677.ch12.ch12fig06
Figure 6
Developmental phenotype of the carD and carG mutants. Photographs were taken after 5-day incubation of 10-μl droplets of cells (1.25 × 108 cells/ml) spotted on CF agar. The wild-type control strain is DK1622.
10.1128/9781555815677/f0221-01_thmb.gif
10.1128/9781555815677/f0221-01.gif
Figure 6
Developmental phenotype of the carD and carG mutants. Photographs were taken after 5-day incubation of 10-μl droplets of cells (1.25 × 108 cells/ml) spotted on CF agar. The wild-type control strain is DK1622.
Citation:
Elías-Arnanz M, Fontes M, Padmanabhan S.
2008.
12 Carotenogenesis in Myxococcus xanthus: a Complex Regulatory Network,
p 211-225.
In
Whitworth D (ed),
Myxobacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555815677.ch12
References
/content/book/10.1128/9781555815677.ch12
1.
Armstrong, G. A. 1997. Genetics of eubacterial carotenoid synthesis: a colourful tale. Annu. Rev. Microbiol. 51: 629– 659.
2.
Balsalobre, J. M. 1989. Inducción por la luz de la expresión génica y la carotenogénesis en Myxococcus xanthus. Ph.D. thesis. University of Murcia, Murcia, Spain.
3.
Balsalobre, J. M.,, R. M. Ruiz-Vázquez, and, F. J. Murillo. 1987. Light induction of gene expression in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 84: 2359– 2362.
4.
Bauer, C.,, S. Essen,, L. R. Swem,, D. L. Swem, and, S. Masuda. 2002. Redox and light regulation of gene expression in photosynthetic prokaryotes. Philos. Trans. R. Soc. Lond. B 358: 147– 154.
5.
Botella, J. A.,, R. M. Ruiz-Vázquez, and, F. J. Murillo, 1995. A cluster of structural and regulatory genes for light-induced carotenogenesis in Myxococcus xanthus. Eur. J. Biochem. 223: 238– 248.
6.
Bramley, P. M., and, A. Mackenzie. 1988. Regulation of carotenoid biosynthesis. Curr. Top. Cell. Regul. 29: 291– 343.
7.
Brown, N. L.,, J. V. Stoyanov,, S. P. Kidd, and, J. L. Hobman, 2003. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27: 145– 163.
8.
Browning, D. F.,, D. E. Whitworth, and, D. A. Hodgson, 2003. Light-induced carotenogenesis in Myxococcus xanthus: functional characterization of the ECF sigma factor CarQ and antisigma factor CarR. Mol. Microbiol. 48: 237– 251.
9.
Burchard, R. P., and, M. Dworkin. 1966. Light-induced lysis and carotenogenesis in Myxococcus xanthus. J. Bacteriol. 91: 535– 545.
10.
Burchard, R. P.,, S. A. Gordon, and, M. Dworkin. 1966. Action spectrum for the photolysis of Myxococcus xanthus. J. Bacteriol. 91: 896– 897.
11.
Burchard, R. P., and, S. P. Hendricks, 1969. Action spectrum for carotenogenesis in Myxococcus xanthus. J. Bacteriol. 97: 1665– 1668.
12.
Cayuela, M. L.,, M. Elías-Arnanz,, M. Peñalver-Mellado,, S. Padmanabhan, and, F. J. Murillo. 2003. The Stigmatella aurantiaca homolog of Myxococcus xanthus high-mobility-group A-type transcription factor CarD: insights into the functional modules of CarD and their distribution in bacteria. J. Bacteriol. 185: 3527– 3537.
13.
Cervantes, M. 2000. Acción de genes estructurales y reguladores en la respuesta a la luz azul de Myxococcus xanthus. Ph.D. thesis. University of Murcia, Murcia, Spain.
14.
Cervantes, M., and, F. J. Murillo, 2002. Role for vitamin B 12 in light induction of gene expression in the bacterium Myxococcus xanthus. J. Bacteriol. 184: 2215– 2224.
15.
Díaz-Perales, A.,, V. Quesada,, J. R. Peinado,, A. P. Ugalde,, J. Álvarez,, M. F. Suárez,, F. X. Gomis-Rüth, and, C. López-Otín. 2005. Identification and characterization of human archaemetzincin–1 and –2, two novel members of a family of metalloproteases widely distributed in Archaea. J. Biol. Chem. 280: 30367– 30375.
16.
Fontes, M.,, L. Galbis-Martínez, and, F. J. Murillo. 2003. A novel regulatory gene for light-induced carotenoid synthesis in the bacterium Myxococcus xanthus. Mol. Microbiol. 47: 561– 571.
17.
Fontes, M.,, R. M. Ruiz-Vázquez, and, F. J. Murillo. 1993. Growth-phase dependence of the activation of a bacterial gene for carotenoid synthesis by blue light. EMBO J. 12: 1265– 1275.
18.
Frank, H. A., and, G. W. Brudvig, 2004. Redox functions of carotenoids in photosynthesis. Biochemistry 43: 8607– 8615.
19.
Friedman, D. I. 1988. Integration host factor: a protein for all reasons. Cell 55: 545– 554.
20.
Galbis-Martínez, L. 2005. Análisis genético y molecular de un transductor de la señal luminosa en la bacteria Myxococcus xanthus. Ph.D. thesis. University of Murcia, Murcia, Spain.
21.
Galbis-Martínez, M.,, M. Fontes, and, F. J. Murillo. 2004. The high-mobility group A-type protein of the bacterium Myxococcus xanthus as a transcription factor for several distinct vegetative genes. Genetics 167: 1585– 1595.
22.
Goodwin, T. W. 1980. The Biochemistry of Carotenoids, vol. 1. Plants. Chapman and Hall, Ltd., London, United Kingdom.
23.
Gorham, H. C.,, S. J. McGowan,, P. R. H. Robson, and, D. A. Hodgson. 1996. Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol. Microbiol. 48: 237– 251.
24.
Henne, A., et al. 2004. The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 22: 547– 553.
25.
Hodgson, D. A. 1993. Light-induced carotenogenesis in Myxococcus xanthus: genetic analysis of the carR region. Mol. Microbiol. 7: 471– 488.
26.
Hodgson, D. A., and, A. E. Berry, 1998. Light regulation of carotenoid synthesis in Myxococcus xanthus, p. 185– 211. In M. X. Caddick,, S. Baumberg,, D. A. Hodgson,, and M. K. Phillips-Jones (ed.), Microbial Responses to Light and Time, Society for General Microbiology Symposium, vol. 56. Cambridge University Press, Cambridge, United Kingdom.
27.
Hodgson, D. A., and, F. J. Murillo. 1993. Genetics of regulation and pathway of synthesis of carotenoids, p. 157– 181. In M. Dworkin, and D. Kaiser (ed.), Myxobacteria II. American Society for Microbiology, Washington, DC.
28.
Hoshino, T.,, R. Fujii, and, T. Nakahara. 1993. Molecular cloning and sequence analysis of the crtB gene of Thermus thermophilus HB27, an extreme thermophile producing carotenoid pigments. Appl. Environ. Microbiol. 58: 93– 98.
29.
Hughes, K. T., and, K. Mathee. 1998. The anti-sigma factors. Annu. Rev. Microbiol. 52: 231– 286.
30.
Iniesta, A. A. 2003. Expresión de genes carotenogénicos de la bacteria Myxococcus xanthus en Escherichia coli. Ph.D. thesis. University of Murcia, Murcia, Spain.
31.
Jarrett, J. T.,, C. W. Goulding,, K. Fluhr,, S. Huang, and, R. G. Matthews. 1997. Purification and assay of cobalamin-dependent methionine synthase from Escherichia coli. Methods Enzymol. 281: 196– 213.
32.
Kaiser, D. 2003. Coupling cell movement to multicellular development in myxobacteria. Nat. Rev. Microbiol. 1: 45– 54.
33.
Kaiser, D. 2004. Signaling in myxobacteria. Annu. Rev. Microbiol. 58: 75– 98.
34.
Kato, F.,, T. Hino,, A. Nakaji,, M. Tanaka, and, Y. Koyama. 1995. Carotenoid synthesis in Streptomyces setonii ISP5395 is induced by the gene crtS, whose product is similar to a sigma factor. Mol. Gen. Genet. 247: 387– 390.
35.
Kleinig, H. 1972. Membranes from Myxococcus fulvus ( Myxobacterales) containing carotenoid glucosides. Isolation and composition. Biochim. Biophys. Acta 274: 489– 498.
36.
Krubasik P., and, G. Sandmann. 2000. Molecular evolution of lycopene cyclases involved in the formation of carotenoids with ionone end groups. Biochem. Soc. Trans. 28: 806– 810.
37.
Lee, H. S.,, Y. Ohnishi, and, S. Horinouchi. 2001. A sigma B-like factor responsible for carotenoid biosynthesis in Streptomyces griseus. J. Mol. Microbiol. Biotechnol. 3: 95– 101.
38.
Lonetto, M. A.,, K. L. Brown,, K. E. Rudd, and, M. J. Buttner, 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci. USA 91: 7573– 7577.
39.
López-Rubio, J. J.,, M. Elías-Arnanz,, S. Padmanabhan, and, F. J. Murillo. 2002. A repressor-antirepressor pair links two loci controlling light-induced carotenogenesis in Myxococcus xanthus. J. Biol. Chem. 277: 7262– 7270.
40.
López-Rubio, J. J.,, S. Padmanabhan,, J. M. Lázaro,, M. Salas,, F. J. Murillo, and, M. Elías-Arnanz. 2004. Operator design and mechanism for CarA repressor-mediated down-regulation of the photoinducible carB operon in Myxococcus xanthus. J. Biol. Chem. 279: 28945– 28953.
41.
Martínez-Argudo, I.,, R. M. Ruiz-Vázquez, and, F. J. Murillo. 1998. The structure of an ECF-σ-dependent, light-inducible promoter from the bacterium Myxococcus xanthus. Mol. Microbiol. 30: 883– 893.
42.
Martínez-Laborda, A.,, J. M. Balsalobre,, M. Fontes, and, F. J. Murillo. 1990. Accumulation of carotenoids in structural and regulatory mutants of the bacterium Myxococcus xanthus. Mol. Gen. Genet. 223: 205– 210.
43.
Martínez-Laborda, A.,, M. Elías,, R. Ruiz-Vázquez, and, F. J. Murillo. 1986. Insertion of Tn 5 linked mutations affecting carotenoid synthesis in Myxococcus xanthus. Mol. Gen. Genet. 205: 107– 114.
44.
Martínez-Laborda, A., and, F. J. Murillo. 1989. Genic and allelic interactions in the carotenogenic response of Myxococcus xanthus to blue light. Genetics 122: 481– 490.
45.
Masuda, S., and, C. E. Bauer, 2002. AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110: 613– 623.
46.
McGowan, S. J.,, H. C. Gorham, and, D. A. Hodgson, 1993. Light-induced carotenogenesis in Myxococcus xanthus: DNA sequence analysis of the carR region. Mol. Microbiol. 10: 713– 735.
47.
Meiser, P.,, H. B. Bode, and, R. Muller. 2006. The unique DKxanthene secondary metabolite family from the myxobacterium Myxococcus xanthus is required for developmental sporulation. Proc. Natl. Acad. Sci. USA 103: 19128– 19133.
48.
Moraleda-Muñoz, A.,, J. Pérez,, M. Fontes,, F. J. Murillo, and, J. Muñoz-Dorado. 2005. Copper induction of carotenoid synthesis in the bacterium Myxococcus xanthus. Mol. Microbiol. 56: 1159– 1168.
49.
Moreno, A. J.,, M. Fontes, and, F. J. Murillo. 2001. ihfA gene of the bacterium Myxococcus xanthus and its role in activation of carotenoid genes by blue light. J. Bacteriol. 183: 557– 569.
50.
Moskvin, O. V.,, L. Gomelsky, and, M. Gomelsky. 2005. Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development. J. Bacteriol. 187: 2148– 2156.
51.
Nash, H. A. 1996. The HU and IHF proteins: accessory factors for complex DNA assemblies, p. 149– 179. In E. C. C. Lin, and A. S. Lynch (ed.), Regulation of Gene Expression in Escherichia coli. R. G. Landes Company, Austin, TX.
52.
Navarro-Avilés, G.,, M. A. Jiménez,, M. C. Pérez-Marín,, C. González,, M. Rico,, F. J. Murillo,, M. Elías-Arnanz, and, S. Padmanabhan. 2007. Structural basis for operator and anti-repressor recognition by Myxococcus xanthus CarA repressor. Mol. Microbiol. 63: 980– 994.
53.
Nicolás, F. J.,, M. L. Cayuela,, I. M. Martínez-Argudo,, R. M. Ruiz-Vázquez, and, F. J. Murillo. 1996. High mobility group I(Y)-like DNA-binding domains on a bacterial transcription factor. Proc. Natl. Acad. Sci. USA 93: 6881– 6885.
54.
Nicolás, F. J.,, R. M. Ruiz-Vázquez, and, F. J. Murillo. 1994. A genetic link between light response and multicellular development in the bacterium Myxococcus xanthus. Genes Dev. 8: 2375– 2387.
55.
Padmanabhan, S.,, M. Elías-Arnanz,, E. Carpio,, P. Aparicio, and, F. J. Murillo. 2001. Domain architecture of a high mobility group A-type bacterial transcriptional factor. J. Biol. Chem. 276: 41566– 41575.
56.
Peñalver-Mellado, M.,, F. García-Heras, S., Padmanabhan, D. García-Moreno,, F. J. Murillo, and, M. Elías-Arnanz. 2006. Recruitment of a novel zinc-bound transcriptional factor by a bacterial HMGA-type protein is required for regulating multiple processes in Myxococcus xanthus. Mol. Microbiol. 61: 910– 926.
57.
Pérez-Marín, M. C.,, J. J. López-Rubio,, F. J. Murillo,, M. Elías-Arnanz, and, S. Padmanabhan. 2004. The N-terminus of Myxococcus xanthus CarA repressor is an autonomously folding domain that mediates physical and functional interactions with both operator DNA and antirepressor protein. J. Biol. Chem. 279: 33093– 33103.
58.
Reeves, R. 2001. Molecular biology of HMGA proteins: hubs of nuclear function. Gene 277: 63– 81.
59.
Reeves, R. 2003. HMGA proteins: flexibility finds a nuclear niche. Biochem. Cell Biol. 81: 185– 195.
60.
Reichenbach, H., and, H. Kleinig. 1984. Pigments of myxobacteria, p. 128– 137. In E. Rosenberg (ed.), Myxobacteria: Development and Cell Interactions. Springer-Verlag, New York, NY.
61.
Robson, P., R. H. 1992. Towards a Mechanism of Caroteno-genesis in Myxococcus xanthus. Ph.D. thesis. University of Warwick, Coventry, England.
62.
Ruiz-Vázquez, R. M.,, M. Fontes, and, F. J. Murillo. 1993. Clustering and co-ordinated activation of carotenoid genes in Myxococcus xanthus by blue light. Mol. Microbiol. 10: 25– 34.
63.
Schumann, G.,, H. Nurnberger,, G. Sandmann, and, H. Krugel. 1996. Activation and analysis of cryptic crt genes for carotenoid biosynthesis from Streptomyces griseus. Mol. Gen. Genet. 252: 658– 666.
64.
Takano, H.,, D. Asker,, T. Beppu, and, K. Ueda. 2006a. Genetic control for light-induced carotenoid production in nonphototrophic bacteria. J. Ind. Microbiol. Biotechnol. 33: 88– 93.
65.
Takano, H.,, T. Beppu, and, K. Ueda. 2006b. The CarA/LitR-family transcriptional regulator: its possible role as a photosensor and wide distribution in non-phototrophic bacteria. Biosci. Biotechnol. Biochem. 70: 2320– 2324.
66.
Takano, H.,, S. Obitsu,, T. Beppu, and, K. Ueda. 2005. Light-induced carotenogenesis in Streptomyces coelicolor A3(2): identification of an extracytoplasmic function sigma factor that directs photodependent transcription of the carotenoid biosynthesis gene cluster. J. Bacteriol. 187: 1825– 1832.
67.
Takayama, F.,, T. Egashira, and, Y. Yamanaka. 2001. Singlet oxygen generation from phosphatidylcholine hydroperoxide in the presence of copper. Life Sci. 68: 1807– 1815.
68.
Whitworth, D. E.,, S. J. Bryan,, A. E. Berry,, S. J. McGowan, and, D. A. Hodgson, 2004. Genetic dissection of the light-inducible carQRS promoter region of Myxococcus xanthus. J. Bacteriol. 186: 7836– 7846.
69.
Whitworth, D. E., and, D. A. Hodgson, 2001. Light-induced carotenogenesis in Myxococcus xanthus: evidence that CarS acts as an anti-repressor of CarA. Mol. Microbiol. 42: 809– 819.