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. 2002 Nov 12;99(23):14913-8.
doi: 10.1073/pnas.192558999. Epub 2002 Oct 28.

Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach

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Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach

Nitin S Baliga et al. Proc Natl Acad Sci U S A. .

Abstract

The extremely halophilic archaeon Halobacterium NRC-1 can switch from aerobic energy production (energy from organic compounds) to anaerobic phototrophy (energy from light) by induction of purple membrane biogenesis. The purple membrane is made up of multiple copies of a 1:1 complex of bacterioopsin (Bop) and retinal called bacteriorhodopsin that functions as a light-driven proton pump. A light- and redox-sensing transcription regulator, Bat, regulates critical genes encoding the biogenesis of the purple membrane. To better understand the regulatory network underlying this physiological state, we report a systems approach using global mRNA and protein analyses of four strains of Halobacterium sp.: the wild-type, NRC-1; and three genetically perturbed strains: S9 (bat+), a purple membrane overproducer, and two purple membrane deficient strains, SD23 (a bop knockout) and SD20 (a bat knockout). The integrated DNA microarray and proteomic data reveal the coordinated coregulation of several interconnected biochemical pathways for phototrophy: isoprenoid synthesis, carotenoid synthesis, and bacteriorhodopsin assembly. In phototrophy, the second major biomodule for ATP production, arginine fermentation, is repressed. The primary systems level insight provided by this study is that two major energy production pathways in Halobacterium sp., phototrophy and arginine fermentation, are inversely regulated, presumably to achieve a balance in ATP production under anaerobic conditions.

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Figures

Fig 1.
Fig 1.
Microarray analysis of wild-type (NRC-1) Halobacterium sp. and three mutants: S9 (bat overexpression), SD20 (bat knockout), and SD23 (bop knockout). Scatter plots on average median-normalized intensities (μx and μy) for three microarray comparisons: (a) bat+ vs. wild type; (b) bat+ vs. bat−; and (c) bat+ vs. bop−. Representative data points (black dots) with significant differential expression (λ > 18) are labeled. (d) Northern blot analysis on 5 (lanes 1 and 3) and 10 μg (lanes 2 and 4) of total RNA for two representative genes involved in arginine degradation (arcC) and arginine synthesis (argG).
Fig 2.
Fig 2.
A comparison of mRNA and protein expression patterns. The diagonal indicates a 1:1 correspondence.
Fig 3.
Fig 3.
Promoter analysis on functionally linked and coordinately coregulated genes. (a) Sequence logo for the four occurrences of the UAS in Halobacterium NRC-1 genome is aligned with the likely UAS upstream to mvaA. The corresponding location and consensus sequence of the bop promoter TATA box are shown. An alternate position of a potential TATA box sequence upstream to the mvaA UAS is boxed. (b) Gene name, strand (±), relative location from the start codon, P value, and sequence for the motif occurrences are shown. (c) Sequence logo for the motif alignment in b. A cosine curve with a periodicity of one helical turn (≈10 bp) is overlaid on the sequence logo.
Fig 4.
Fig 4.
The bR regulon and the isoprenoid, carotenoid, and bR biomodules in Halobacterium sp. (6, 8, 21). (a) The bR regulon. Genes shaded in red are transcriptionally regulated by Bat. (b) The isoprenoid, carotenoid, and bR biomodules. Pink shading indicates up-regulation, and green denotes down-regulation in the bat− strain relative to the bat+ strain. The intermediates and enzymes catalyzing the various biochemical conversions are indicated with ratios of mRNA or protein levels in the bat− strain relative to the bat+ strain in parentheses. A question mark (?) indicates that the enzyme catalyzing the reaction has yet to be identified. The multiple arrows from IPP to GGPP indicate this conversion requires several steps (22). The red lines and arrows indicate enzymatic steps regulated transcriptionally by Bat. The dashed lines within the bR biomodule indicate positive (+ve) or negative (−ve) feedback loops controlling conversion of lycopene to β-carotene (7).
Fig 5.
Fig 5.
The arginine synthesis and fermentation biomodule in Halobacterium sp. The enzymes are indicated, with message or protein expression ratios in the bat− to bat+ strains in parentheses. Green shading indicates down-regulation and pink denotes up-regulation in the bat− to bat+ strain comparisons.

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