Betaine Use by Rhizosphere Bacteria: Genes Essential for Trigonelline, Stachydrine, and Carnitine Catabolism in<i>Rhizobium meliloti</i>Are Located on pSym in the Symbiotic Region

Goldmann, Arlette; Boivin, C.; fleury,; Message, Brigitte; L, Lecoeur; Maille, M.; Tepfer, David

doi:10.1094/mpmi-4-571

Cited by 72 publications

(63 citation statements)

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“…Since substantial radioactivity remained in the supernatants of the cultures even after 16 h of growth in the presence of [methyl- 14 C]choline, we analyzed the nature of the radiolabelled compounds by thin-layer chromatography (Fig. 2B).…”

Section: Vol 178 1996 Glycine Betaine Synthesis In B Subtilis 5123mentioning

confidence: 99%

“…2B). Only [methyl- 14 C]choline could be found in the supernatants of the cultures of strains deficient in glycine betaine synthesis (Fig. 2B, lanes 1, 2, 7, and 8), indicating that this compound either was not taken up completely or leaked from the bacterial cells once it had been accumulated.…”

Section: Vol 178 1996 Glycine Betaine Synthesis In B Subtilis 5123mentioning

confidence: 99%

“…It is synthesized by plants and is thus brought into the habitat of B. subtilis through the degradation of plant tissues and root exudates (14,44). Glycine betaine can be accumulated directly from the environment through three osmotically controlled uptake systems (25): OpuD, a single-component transporter, and OpuA and OpuC (ProU), multicomponent transport systems that are related to the binding protein-dependent transport system ProU from Escherichia coli (25,26,34).…”

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Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes

et al. 1996

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Synthesis of the osmoprotectant glycine betaine from the exogenously provided precursor choline or glycine betaine aldehyde confers considerable osmotic stress tolerance to Bacillus subtilis in high-osmolarity media. Using an Escherichia coli mutant (betBA) defective in the glycine betaine synthesis enzymes, we cloned by functional complementation the genes that are required for the synthesis of the osmoprotectant glycine betaine in B. subtilis. The DNA sequence of a 4.1-kb segment from the cloned chromosomal B. subtilis DNA was established, and two genes (gbsA and gbsB) whose products were essential for glycine betaine biosynthesis and osmoprotection were identified. The gbsA and gbsB genes are transcribed in the same direction, are separated by a short intergenic region, and are likely to form an operon. The deduced gbsA gene product exhibits strong sequence identity with members of a superfamily of specialized and nonspecialized aldehyde dehydrogenases. This superfamily comprises glycine betaine aldehyde dehydrogenases from bacteria and plants with known involvement in the cellular adaptation to high-osmolarity stress and drought. The deduced gbsB gene product shows significant similarity to the family of type III alcohol dehydrogenases. B. subtilis mutants with defects in the chromosomal gbsAB genes were constructed by marker replacement, and the growth properties of these mutant strains in high-osmolarity medium were analyzed. Deletion of the gbsAB genes destroyed the cholineglycine betaine synthesis pathway and abolished the ability of B. subtilis to deal effectively with high-osmolarity stress in choline-or glycine betaine aldehyde-containing medium. Uptake of radiolabelled choline was unaltered in the gbsAB mutant strain. The continued intracellular accumulation of choline or glycine betaine aldehyde in a strain lacking the glycine betaine-biosynthetic enzymes strongly interfered with the growth of B. subtilis, even in medium of moderate osmolarity. A single transcription initiation site for gbsAB was detected by high-resolution primer extension analysis. gbsAB transcription was initiated from a promoter with close homology to A -dependent promoters and was stimulated by the presence of choline in the growth medium.

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Section: Vol 178 1996 Glycine Betaine Synthesis In B Subtilis 5123mentioning

confidence: 99%

Section: Vol 178 1996 Glycine Betaine Synthesis In B Subtilis 5123mentioning

confidence: 99%

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Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes

et al. 1996

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“…However, both the two dehydrogenases and the oxidase possess, at their N-terminus, a ' glycine box ' containing a conserved motif (GXGXXG) and a series of amino acids which are characteristic features of flavoproteins (Wierenga et al, 1986;Hanukoglu & Gutfinger, 1989;Lamark et al, 1991 Symbiotic proficiency of LTS23-1020 and genomic location of the betBA genes Besides the chromosome, S. meliloti contains two symbiotic megaplasmids called pSyma and pSymb (Burkhardt et al, 1987;Sobral et al, 1991). Genes essential for the catabolism of at least three betaines, carnitine, trigonelline and stachydrine (proline betaine) , map near the nod region of pSyma in S. meliloti RCR2011 (Goldman et al, 1991). stc (stachydrine catabolism) mutants show delayed and reduced nodulation patterns (Goldman et al, 1994), and genes encoding the catabolism of trigonelline are expressed throughout the Sinorhizobium/alfalfa symbiosis (Boivin et al, 1990).…”

Section: Nucleotide Sequence Of the Betba Genesmentioning

confidence: 99%

Molecular characterization of the bet genes encoding glycine betaine synthesis in Sinorhizobium meliloti 102F34

et al. 1997

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As a first step towards the elucidation of the molecular mechanisms responsible for the utilization of choline and glycine betaine (betaine) either as carbon and nitrogen sources or as osmoprotectants in Sinorhizobium meliloti, we selected a T n 5 mutant, LTS23-1020, which failed to grow on choline but grew on betaine. The mutant was deficient in choline dehydrogenase (CDH) activity, failed to oxidize [methyl-14C]choline to [methyl-I4C]betaine, and did not use choline, but still used betaine, as an osmoprotectant. The T n 5 mutation in LTS23-1020 was complemented by plasmid pCH034, isolated from a genomic bank of 5. meliloti 102F34. Subcloning and DNA sequencing showed that pCH034 harbours two ORFs which showed 60% and 57% identity with the Escherichia coli betB gene encoding betaine-aldehyde dehydrogenase (BADH) and betA gene encoding CDH, respectively. In addition to the homology with E. coli genes, the deduced sequence of the sinorhizobial BADH protein displays consensus sequences also found in plant BADHs. The deduced sequence of the sinorhizobial CDH protein shares only 21 O/ O identical residues with choline oxidase from Atthrobacter globiformis. The structural organization of the betBA genes in S. meliloti differs from that described in E. coli: (i) the two ORFs are separated by a 210 bp sequence containing inverted repeats ressembling a putative rhoindependent transcription terminator, and (ii) no sequence homologous to betT (high-aff inity choline transport system) or bet/ (regulator) was found in the vicinity of the sinorhizobial betBA genes. Evidence is also presented that the S. meliloti betBA genes are not located on the megaplasmids.

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“…Interestingly, S. meliloti transports this betaine by a high-affinity Na 1 -coupled transporter, BetS (Boscari et al, 2002), and via an ABC (ATP-binding cassette) protein-dependent transporter, Hut (Boncompagni et al, 2000). In addition, S. meliloti uses Pro betaine as a carbon and nitrogen source or as an osmoprotectant (Gloux and Le Rudulier, 1989;Goldmann et al, 1991;Burnet et al, 2000). Given the competition among soil bacteria for plant carbon sources, it is interesting to point out that Pro betaine catabolism contributes to rhizobial colonization of seedling roots (Phillips et al, 1998).…”

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Proline Betaine Accumulation and Metabolism in Alfalfa Plants under Sodium Chloride Stress. Exploring Its Compartmentalization in Nodules

et al. 2004

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The osmoprotectant Pro betaine is the main betaine identified in alfalfa (Medicago sativa). We have investigated the long-term responses of nodulated alfalfa plants to salt stress, with a particular interest for Pro betaine accumulation, compartmentalization, and metabolism. Exposure of 3-week-old nodulated alfalfa plants to 0.2 m NaCl for 4 weeks was followed by a 10-, 4-, and 8-fold increase in Pro betaine in shoots, roots, and nodules, respectively. Isotope-labeling studies in alfalfa shoots indicate that [14C]Pro betaine was synthesized from l-[14C]Pro. [14C]Pro betaine was efficiently catabolized through sequential demethylations via N-methylPro and Pro. Salt stress had a minor effect on Pro betaine biosynthesis, whereas it strongly reduced Pro betaine turnover. Analysis of Pro betaine and Pro compartmentalization within nodules revealed that 4 weeks of salinization of the host plants induced a strong increase in cytosol and bacteroids. The estimated Pro betaine and Pro concentrations in salt-stressed bacteroids reached 7.4 and 11.8 mm, respectively, compared to only 0.8 mm in control bacteroids. Na+ content in nodule compartments was also enhanced under salinization, leading to a concentration of 14.7 mm in bacteroids. [14C]Pro betaine and [14C]Pro were taken up by purified symbiosomes and free bacteroids. There was no indication of saturable carrier(s), and the rate of uptake was moderately enhanced by salinization. Ultrastructural analysis showed a large peribacteroid space in salt-stressed nodules, suggesting an increased turgor pressure inside the symbiosomes, which might partially be due to an elevated concentration in Pro, Pro betaine, and Na+ in this compartment.

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Betaine Use by Rhizosphere Bacteria: Genes Essential for Trigonelline, Stachydrine, and Carnitine Catabolism inRhizobium melilotiAre Located on pSym in the Symbiotic Region

Cited by 72 publications

References 0 publications

Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes

Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: characterization of the gbsAB genes

Molecular characterization of the bet genes encoding glycine betaine synthesis in Sinorhizobium meliloti 102F34

Proline Betaine Accumulation and Metabolism in Alfalfa Plants under Sodium Chloride Stress. Exploring Its Compartmentalization in Nodules

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