The <i>Sinorhizobium meliloti</i> Glycine Betaine Biosynthetic Genes (<i>betICBA</i>) Are Induced by Choline and Highly Expressed in Bacteroids

Mandon, Karine; Østerås, Magne; Boncompagni, Éric; Trinchant, Jean-Charles; Spennato, Guillaume; Poggi, Marie Christine; Rudulier, Daniel Le

doi:10.1094/mpmi.2003.16.8.709

Cited by 43 publications

(36 citation statements)

References 42 publications

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“…These genes also have well-supported orthologues in all other pseudomonads (www.pseudomonas.com). Apart from the identification of a novel GB demethylase system based on a monooxygenase, this pathway is similar to that described for other choline degraders, particularly in the Rhizobiaceae (81,82).…”

Section: Regulation Of Aerobic Choline and Gb Catabolism In Pseudomonadsmentioning

confidence: 55%

Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

Wargo

2013

Appl Environ Microbiol

156

121

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Most sequenced bacteria possess mechanisms to import choline and glycine betaine (GB) into the cytoplasm. The primary role of choline in bacteria appears to be as the precursor to GB, and GB is thought to primarily act as a potent osmoprotectant. Choline and GB may play accessory roles in shaping microbial communities, based on their limited availability and ability to enhance survival under stress conditions. Choline and GB enrichment near eukaryotes suggests a role in the chemical relationships between these two kingdoms, and some of these interactions have been experimentally demonstrated. While many bacteria can convert choline to GB for osmoprotection, a variety of soil-and water-dwelling bacteria have catabolic pathways for the multistep conversion of choline, via GB, to glycine and can thereby use choline and GB as sole sources of carbon and nitrogen. In these choline catabolizers, the GB intermediate represents a metabolic decision point to determine whether GB is catabolized or stored as an osmo-and stress protectant. This minireview focuses on this decision point in Pseudomonas aeruginosa, which aerobically catabolizes choline and can use GB as an osmoprotectant and a nutrient source. P. aeruginosa is an experimentally tractable and ecologically relevant model to study the regulatory pathways controlling choline and GB homeostasis in choline-catabolizing bacteria. The study of P. aeruginosa associations with eukaryotes and other bacteria also makes this a powerful model to study the impact of choline and GB, and their associated regulatory and catabolic pathways, on host-microbe and microbe-microbe relationships.

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Section: Regulation Of Aerobic Choline and Gb Catabolism In Pseudomonadsmentioning

confidence: 55%

Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

Wargo

2013

Appl Environ Microbiol

156

121

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“…Genes involved in choline uptake and metabolism in S. meliloti are highly expressed under symbiotic conditions (14,28). To further inspect the link between virulence and PC biosynthesis in A. tumefaciens, we tested if virulence conditions change the expression of the PC biosynthesis genes.…”

Section: Resultsmentioning

confidence: 99%

Expression and Physiological Relevance of Agrobacterium tumefaciens Phosphatidylcholine Biosynthesis Genes

et al. 2009

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Phosphatidylcholine (PC), or lecithin, is the major phospholipid in eukaryotic membranes, whereas only 10% of all bacteria are predicted to synthesize PC. In Rhizobiaceae, including the phytopathogenic bacterium Agrobacterium tumefaciens, PC is essential for the establishment of a successful host-microbe interaction. A. tumefaciens produces PC via two alternative pathways, the methylation pathway and the Pcs pathway. The responsible genes, pmtA (coding for a phospholipid N-methyltransferase) and pcs (coding for a PC synthase), are located on the circular chromosome of A. tumefaciens C58. Recombinant expression of pmtA and pcs in Escherichia coli revealed that the individual proteins carry out the annotated enzyme functions. Both genes and a putative ABC transporter operon downstream of PC are constitutively expressed in A. tumefaciens. The amount of PC in A. tumefaciens membranes reaches around 23% of total membrane lipids. We show that PC is distributed in both the inner and outer membranes. Loss of PC results in reduced motility and increased biofilm formation, two processes known to be involved in virulence. Our work documents the critical importance of membrane lipid homeostasis for diverse cellular processes in A. tumefaciens.

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“…3B). Since choline is a ubiquitous molecule in plants and has been identified in alfalfa nodules (18), we wanted to determine whether this transporter was present in bacteroids. Therefore, bacteroids from nodules produced on M. sativa roots by strains Rm5000 and M1A were purified, and the ChoX protein level was estimated by immunoblotting.…”

Section: Resultsmentioning

confidence: 99%

“…The symbiotic proficiency of S. meliloti strains was assayed by using alfalfa (M. sativa L. cv. Europe) seedlings grown in a sterilized mixture of vermiculite and sand and inoculated with the appropriate strains 1 week after sowing, as described previously (18). The number and the mass of nodules were determined 3, 5, 6, and 7 weeks after inoculation.…”

Section: Methodsmentioning

confidence: 99%

The Sinorhizobium meliloti ABC Transporter Cho Is Highly Specific for Choline and Expressed in Bacteroids from Medicago sativa Nodules

et al. 2004

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In Sinorhizobium meliloti, choline is the direct precursor of phosphatidylcholine, a major lipid membrane component in the Rhizobiaceae family, and glycine betaine, an important osmoprotectant. Moreover, choline is an efficient energy source which supports growth. Using a PCR strategy, we identified three chromosomal genes (choXWV) which encode components of an ABC transporter: ChoX (binding protein), ChoW (permease), and ChoV (ATPase). Whereas the best homology scores were obtained with components of betaine ProU-like systems, Cho is not involved in betaine transport. Site-directed mutagenesis of choX strongly reduced (60 to 75%) the choline uptake activity, and purification of ChoX, together with analysis of the ligand-binding specificity, showed that ChoX binds choline with a high affinity (K D , 2.7 M) and acetylcholine with a low affinity (K D , 145 M) but binds none of the betaines. Uptake competition experiments also revealed that ectoine, various betaines, and choline derivatives were not effective competitors for Cho-mediated choline transport. Thus, Cho is a highly specific high-affinity choline transporter. Choline transport activity and ChoX expression were induced by choline but not by salt stress. Western blotting experiments with antibodies raised against ChoX demonstrated the presence of ChoX in bacteroids isolated from nitrogen-fixing nodules obtained from Medicago sativa roots. The choX mutation did not have an effect on growth under standard conditions, and neither Nod nor Fix phenotypes were impaired in the mutant, suggesting that the remaining choline uptake system(s) still present in the mutant strain can compensate for the lack of Cho transporter.Choline is a common constituent of eukaryotic membranes in the form of phosphatidylcholine (PC) and therefore should be widespread in different environments, including the soil and the rhizosphere. Indeed, significant amounts of choline are readily liberated into the environment from plant and animal residues (15). Sinorhizobium meliloti, a plant root-associated bacterium, possesses distinct transport activities for choline uptake (27) and has the ability to oxidize choline to glycine betaine via the bet operon (34,24). In contrast to Escherichia coli and Bacillus subtilis (25, 2), S. meliloti can use choline for growth. This depends on a functional bet locus (34, 24) associated with catabolism of glycine betaine which is absent in E. coli and B. subtilis. This catabolism is reduced under hyperosmotic conditions, and under these conditions glycine betaine accumulation is favored (34). Moreover, due to the presence of a PC synthase in S. meliloti, which directly condenses choline to CDP-diacylglyceride, choline is a direct precursor of PC, as recently demonstrated for other bacteria, including Agrobacterium, Brucella, and Pseudomonas (6,19). In addition to this PC synthase pathway, S. meliloti possesses a methylation pathway for PC biosynthesis which functions by threefold methylation of phosphatidylethanolamine with S-adenosylmethionine as a methy...

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The Sinorhizobium meliloti Glycine Betaine Biosynthetic Genes (betICBA) Are Induced by Choline and Highly Expressed in Bacteroids

Cited by 43 publications

References 42 publications

Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

Expression and Physiological Relevance of Agrobacterium tumefaciens Phosphatidylcholine Biosynthesis Genes

The Sinorhizobium meliloti ABC Transporter Cho Is Highly Specific for Choline and Expressed in Bacteroids from Medicago sativa Nodules

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