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12 Carotenogenesis in : a Complex Regulatory Network

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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 . The observation that the action spectra for photolysis and carotenogenesis in 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 gene was identified in a screen for Car mutants among a large collection of strains bearing Tn insertions. Recent studies have identified a new factor, CarG (the product of the gene directly downstream of ), which is required in every CarD-dependent process analyzed. The CarA operator design and the mechanism underlying the repression-antirepression switch of P have been subjected to detailed molecular analysis. The most studied phenomenon in 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 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 : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12

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Figures

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Figure 1

Known genetic elements involved in carotenogenesis and their interactions. Squat arrows show photoinducible genes () or operons ( and the 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 , all of the genes in the operon, and and in the 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 : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12
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Image of Figure 2
Figure 2

Carotenoid biosynthetic pathway and the genes involved in each step. The proposed pathway for the biosynthesis of myxobacton, the primary carotenoid in , 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 : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12
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Figure 3

Design of the light-inducible promoters identified in . Sequences show the promoter regions of P, P, and P, the three light-inducible promoters. The –10 and –35 bases are marked for all three promoters. In P, the CarD-binding site is boxed (with the two AT-rich tracts underlined). Two bases at the –35 region of P, which on mutation remove light-induced promoter activity, are underlined (Whitworth et al., 2004). The bases underlined in the P promoter sequence are critical for promoter activity ( ). In the P 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 : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12
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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 : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12
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Figure 5

Model for the action of CarA and CarS in the regulation of the P 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 . 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 .

Citation: Elías-Arnanz M, Fontes M, Padmanabhan S. 2008. 12 Carotenogenesis in : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12
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Figure 6

Developmental phenotype of the and mutants. Photographs were taken after 5-day incubation of 10-μl droplets of cells (1.25 × 10 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 : a Complex Regulatory Network, p 211-225. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch12
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