Transcriptome Dynamics during the Transition from Anaerobic Photosynthesis to Aerobic Respiration in
            <i>Rhodobacter sphaeroides</i>
            2.4.1

Arai, Hiroyuki; Roh, Jung Hyeob; Kaplan, Samuel

doi:10.1128/jb.01375-07

Cited by 57 publications

(48 citation statements)

References 92 publications

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“…However, it was unexpected that the quadruple mutant strain QXAa was unable to grow aerobically (Fig. 1A), because aa 3 -type oxidases play major roles in aerobic growth in many bacterial species (23)(24)(25)(26). Transcription of the cox genes encoding aa 3 is repressed by the two-component regulator RoxSR and is dependent on the stationary-phase sigma factor RpoS (21).…”

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confidence: 99%

“…aa 3 is closely related to mitochondrial terminal oxidases. aa 3 -type oxidases typically have low affinity for oxygen and function as main enzymes under high-oxygen conditions in many bacterial species (23)(24)(25)(26). However, in P. aeruginosa, aa 3 is expressed at very low levels in nutrient-rich medium under high-oxygen conditions and is upregulated only in response to nutrient starvation (21).…”

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Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

et al. 2014

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The ubiquitous opportunistic pathogen Pseudomonas aeruginosa has five aerobic terminal oxidases: bo 3 -type quinol oxidase (Cyo), cyanide-insensitive oxidase (CIO), aa 3 -type cytochrome c oxidase (aa 3 ), and two cbb 3 -type cytochrome c oxidases (cbb 3 -1 and cbb 3 -2). These terminal oxidases are differentially regulated under various growth conditions and are thought to contribute to the survival of this microorganism in a wide variety of environmental niches. Here, we constructed multiple mutant strains of P. aeruginosa that express only one aerobic terminal oxidase to investigate the enzymatic characteristics and in vivo function of each enzyme. The K m values of Cyo, CIO, and aa 3 for oxygen were similar and were 1 order of magnitude higher than those of cbb 3 -1 and cbb 3 -2, indicating that Cyo, CIO, and aa 3 are low-affinity enzymes and that cbb 3 -1 and cbb 3 -2 are high-affinity enzymes. Although cbb 3 -1 and cbb 3 -2 exhibited different expression patterns in response to oxygen concentration, they had similar K m values for oxygen. Both cbb 3 -1 and cbb 3 -2 utilized cytochrome c 4 as the main electron donor under normal growth conditions. The electron transport chains terminated by cbb 3 -1 and cbb 3 -2 generate a proton gradient across the cell membrane with similar efficiencies. The electron transport chain of aa 3 had the highest proton translocation efficiency, whereas that of CIO had the lowest efficiency. The enzymatic properties of the terminal oxidases reported here are partially in agreement with their regulatory patterns and may explain the environmental adaptability and versatility of P. aeruginosa.

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Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

et al. 2014

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“…The pathways that control transcription of many genes required for the synthesis and function of the photosynthetic apparatus have been extensively studied at the genetic and genomic levels (12)(13)(14)(15). The photosynthesis response regulator (Prr) proteins comprise a two-component signal transduction system activated by low O 2 tension, in which PrrB is a membrane-spanning sensor histidine kinase and PrrA is a DNA-binding response reg-ulator (16,17).…”

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Oxygen-Dependent Regulation of Bacterial Lipid Production

et al. 2015

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Understanding the mechanisms of lipid accumulation in microorganisms is important for several reasons. In addition to providing insight into assembly of biological membranes, lipid accumulation has important applications in the production of renewable fuels and chemicals. The photosynthetic bacterium Rhodobacter sphaeroides is an attractive organism to study lipid accumulation, as it has the ability to increase membrane production at low O 2 tensions. Under these conditions, R. sphaeroides develops invaginations of the cytoplasmic membrane to increase its membrane surface area for housing of the membrane-bound components of its photosynthetic apparatus. Here we use fatty acid levels as a reporter of membrane lipid content. We show that, under low-O 2 and anaerobic conditions, the total fatty acid content per cell increases 3-fold. We also find that the increases in the amount of fatty acid and photosynthetic pigment per cell are correlated as O 2 tensions or light intensity are changed. To ask if lipid and pigment accumulation were genetically separable, we analyzed strains with mutations in known photosynthetic regulatory pathways. While a strain lacking AppA failed to induce photosynthetic pigment-protein complex accumulation, it increased fatty acid content under low-O 2 conditions. We also found that an intact PrrBA pathway is required for low-O 2 -induced fatty acid accumulation. Our findings suggest a previously unknown role of R. sphaeroides transcriptional regulators in increasing fatty acid and phospholipid accumulation in response to decreased O 2 tension. IMPORTANCELipids serve important functions in living systems, either as structural components of membranes or as a form of carbon storage. Understanding the mechanisms of lipid accumulation in microorganisms is important for providing insight into the assembly of biological membranes and additionally has important applications in the production of renewable fuels and chemicals. In this study, we investigate the ability of Rhodobacter sphaeroides to increase membrane production at low O 2 tensions in order to house its photosynthetic apparatus. We demonstrate that this bacterium has a mechanism to increase lipid content in response to decreased O 2 tension and identify a transcription factor necessary for this response. This is significant because it identifies a transcriptional regulatory pathway that can increase microbial lipid content. Lipids serve important functions in living systems, either as structural components of membranes or as a form of carbon storage. Lipids derived from oil-rich microorganisms (including bacteria, yeasts, and microalgae) also offer a promising source of renewable fuels and chemicals (1, 2). However, the genetic and biochemical mechanisms regulating lipid accumulation in microorganisms are poorly understood, have been difficult to study, and are typically linked to stress conditions that hinder growth (3-5). Much effort has been directed at increasing lipid accumulation through alteration of enzymes involved in ...

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“…Rhodobacter sphaeroides 2.4.1 is a purple nonsulfur bacterium which belongs to the Alpha-3-proteobacteria, whose members exhibit diversity in both their morphological and metabolic characteristics. With the availability of its genomic DNA sequence (http://www.rhodobacter.org) and the R. sphaeroides GeneChip (67), transcriptome and proteome analyses have been performed to investigate global cellular expression profiles in response to changes in growth conditions, as well as to the presence of specific mutations (1,5,6,8,9,29,61,72,89).…”

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Regulation of Gene Expression by PrrA in Rhodobacter sphaeroides 2.4.1: Role of Polyamines and DNA Topology

Eraso

Kaplan

2009

J Bacteriol

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In the present study, we show in vitro binding of PrrA, a global regulator in Rhodobacter sphaeroides 2.4.1, to the PrrA site 2, within the RSP3361 locus. Specific binding, as shown by competition experiments, requires the phosphorylation of PrrA. The binding affinity of PrrA for site 2 was found to increase 4-to 10-fold when spermidine was added to the binding reaction. The presence of extracellular concentrations of spermidine in growing cultures of R. sphaeroides gave rise to a twofold increase in the expression of the photosynthesis genes pucB and pufB, as well as the RSP3361 gene, under aerobic growth conditions, as shown by the use of lacZ transcriptional fusions, and led to the production of light-harvesting spectral complexes. In addition, we show that negative supercoiling positively regulates the expression of the RSP3361 gene, as well as pucB. We show the importance of supercoiling through an evaluation of the regulation of gene expression in situ by supercoiling, in the case of the former gene, as well as using the DNA gyrase inhibitor novobiocin. We propose that polyamines and DNA supercoiling act synergistically to regulate expression of the RSP3361 gene, partly by affecting the affinity of PrrA binding to the PrrA site 2 within the RSP3361 gene.

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Transcriptome Dynamics during the Transition from Anaerobic Photosynthesis to Aerobic Respiration in Rhodobacter sphaeroides 2.4.1

Cited by 57 publications

References 92 publications

Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

Oxygen-Dependent Regulation of Bacterial Lipid Production

Regulation of Gene Expression by PrrA in Rhodobacter sphaeroides 2.4.1: Role of Polyamines and DNA Topology

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