scholarly journals Contribution of the β-glucosidase BglC to the Onset of the Pathogenic Lifestyle of Streptomyces scabies

2017 ◽  
Author(s):  
Samuel Jourdan ◽  
Isolde M. Francis ◽  
Benoit Deflandre ◽  
Elodie Tenconi ◽  
Jennifer Riley ◽  
...  

AbstractCommon scab disease on root and tuber plants is caused by Streptomyces scabies and related species which use the cellulose synthase inhibitor thaxtomin A as main phytotoxin. Thaxtomin production is primarily triggered by the import of cello-oligosaccharides. Once inside the cell, the fate of the cello-oligosaccharides is dichotomized into i) fueling glycolysis with glucose for the saprophytic lifestyle through the action of β-glucosidase(s) (BG), and ii) eliciting the pathogenic lifestyle by inhibiting the CebR-mediated transcriptional repression of thaxtomin biosynthetic genes. Here we investigated the role of scab57721 encoding a putative BG (BglC) in the onset of the pathogenicity of S. scabies. Enzymatic assays showed that BglC was able to release glucose from cellobiose, cellotriose and all other cello-oligosaccharides tested. Its inactivation resulted in a phenotype opposite to what was expected as we monitored reduced production of thaxtomin when the mutant was cultivated on media containing cello-oligosaccharides as unique carbon source. This unexpected phenotype could be attributed to the highly increased activity of alternative intracellular BGs, probably as a compensation of bglC inactivation, which then prevented cellobiose and cellotriose accumulation to reduce the activity of CebR. In contrast, when the bglC null mutant was cultivated on media devoid of cello-oligosaccharides it instead constitutively produced thaxtomin. This observed hypervirulent phenotype does not fit with the proposed model of the cello-oligosaccharide-mediated induction of thaxtomin production and suggests that the role of BglC in the route to the pathogenic lifestyle of S. scabies is more complex than currently presented.

2002 ◽  
Vol 48 (4) ◽  
pp. 359-364 ◽  
Author(s):  
Annie Lauzier ◽  
Claudia Goyer ◽  
Luc Ruest ◽  
Ryszard Brzezinski ◽  
Don L Crawford ◽  
...  

The regulatory effect of amino acids on the production of thaxtomin A, a phytotoxin produced by Streptomyces scabies, was investigated. Tryptophan had an important inhibitory effect on the toxin biosynthesis in all five strains of S. scabies tested. Two other aromatic amino acids (tyrosine and phenylalanine) also inhibited thaxtomin A biosynthesis, while aliphatic amino acids did not cause an important decline in thaxtomin A production. Methylation of tryptophan prevented or reduced the inhibitory effect on thaxtomin A biosynthesis. In spite of the inhibitory action of tryptophan and phenylalanine on thaxtomin A production, incorporation of these radiolabeled molecules into thaxtomin A confirmed that they are metabolic precursors for the biosynthesis of the phytotoxin.Key words: thaxtomin A, phytotoxin, Streptomyces scabies, common scab, nitroaromatic compounds, amino acids.


1998 ◽  
Vol 88 (5) ◽  
pp. 442-445 ◽  
Author(s):  
Claudia Goyer ◽  
Joanne Vachon ◽  
Carole Beaulieu

To investigate the role of thaxtomin A in the pathogenicity of Streptomyces scabies, mutants altered in thaxtomin A production were obtained by N-methyl-N′-nitro-N-nitrosoguanidine mutagenesis. Mutants of S. scabies EF-35 could be differentiated according to levels of thaxtomin production. Mutants M1, M8, and M19 produced 2 to 20 times less thaxtomin A in oat bran medium than did EF-35. M1 and M19 were deficient in tryptophan catabolism. Thaxtomin production was reduced by about 300 times in mutant M16, which was a glutamic acid auxotroph. No thaxtomin A was detected in M13 culture supernatant. This mutant had a normal growth rate, was prototrophic, and catabolized tryptophan. Pathogenicity of mutants was tested on radish and potato. Mutants M1, M8, and M19 were pathogenic but, in most cases, less virulent than EF-35. M13 and M16 were nonpathogenic. These results suggest that thaxtomin A is an important pathogenicity determinant in S. scabies.


2004 ◽  
Vol 50 (9) ◽  
pp. 705-709 ◽  
Author(s):  
Julie Beauséjour ◽  
Carole Beaulieu

Streptomyces scabies, a causal agent of common scab, produces both melanin and a secondary metabolite called thaxtomin A. To establish a possible relation between melanin and thaxtomin A production in S. scabies, we carried out N-methyl-N′-nitro-N-nitrosoguanidine (NTG) mutagenesis and isolated 11 melanin-negative mutants of S. scabies EF-35. These mutants were characterized for thaxtomin A production, pathogenicity, sporulation, and stress resistance. Nine of these mutants showed a significant reduction in thaxtomin A production when compared with the wild strain. However, only a few mutants exhibited a reduced level of virulence or a loss in their ability to induce common scab symptoms on potato tubers. Other pleiotrophic effects, such as higher sensitivity to heavy metals and incapacity to sporulate under certain stress conditions, were also associated with a deficiency in melanin production.Key words: common scab, potato, secondary metabolism, stress, thaxtomin.


1999 ◽  
Vol 45 (9) ◽  
pp. 764-768 ◽  
Author(s):  
Julie Beauséjour ◽  
Claudia Goyer ◽  
Joanne Vachon ◽  
Carole Beaulieu

Thaxtomin A production by Streptomyces scabies is induced by plant extracts in culture media. We compared the production of thaxtomin A by three Streptomyces scabies strains (EF-35, CG1, and ATCC 49173) in different culture media in a first attempt to identify the plant molecules required for the biosynthesis of thaxtomin A. Thaxtomin A production varied greatly among media and among S. scabies strains. Strain CG1 presented a higher production than the other strains in all complex media. Oat bran broth is the best thaxtomin A production medium, and suberin is the only plant polymer allowing the production of thaxtomin A in minimal medium. The three S. scabies strains had extracellular esterase activities when grown in the presence of potato suberin or oat bran. We suggest that extracellular esterases allow the release from lipid polymers of plant molecules that may act as inducers for thaxtomin A biosynthesis genes or as precursors in the biosynthetic pathway of thaxtomin A.Key words: common scab, phytotoxin, suberin, esterase.


2015 ◽  
Vol 28 (4) ◽  
pp. 443-454 ◽  
Author(s):  
Joanna K. Fyans ◽  
Mead S. Altowairish ◽  
Yuting Li ◽  
Dawn R. D. Bignell

Streptomyces scabies is an important causative agent of common scab disease of potato tubers and other root crops. The primary virulence factor produced by this pathogen is a phytotoxic secondary metabolite called thaxtomin A, which is essential for disease development. In addition, the genome of S. scabies harbors a virulence-associated biosynthetic gene cluster called the coronafacic acid (CFA)-like gene cluster, which was previously predicted to produce metabolites that resemble the Pseudomonas syringae coronatine (COR) phytotoxin. COR consists of CFA linked to an ethylcyclopropyl amino acid called coronamic acid, which is derived from L-allo-isoleucine. Using a combination of genetic and chemical analyses, we show that the S. scabies CFA-like gene cluster is responsible for producing CFA-L-isoleucine as the major product as well as other minor COR-like metabolites. Production of the metabolites was shown to require the cfl gene, which is located within the CFA-like gene cluster and encodes an enzyme involved in ligating CFA to its amino acid partner. CFA-L-isoleucine purified from S. scabies cultures was shown to exhibit bioactivity similar to that of COR, though it was found to be less toxic than COR. This is the first report demonstrating the production of coronafacoyl phytotoxins by S. scabies, which is the most prevalent scab-causing pathogen in North America.


2016 ◽  
Vol 5 (1) ◽  
pp. 45-51
Author(s):  
Kamal A. M. Abo-Elyousr ◽  
Mohamed Hosny ◽  
Mahmoud R. Asran ◽  
Farag A. Saeed

Streptomyces common scab is one of the most bacterial diseases that costs economic loses to potato plants. Streptomyces scabiei (Thaxter 1891) Lambert and Loria (syn. Streptomyces scabies) is the main causal agent of common scab in potato in the field. Eight potato cultivars namely, Diamont, Lady Rossete, Burna, Lady Bellford, Skenta, Flora, Brofent and Everest were tested for their susceptibility to common scab disease under greenhouse conditions. They varied to some extent in the degree of their susceptibility. Lady Rosette appeared to be the highest susceptible one followed by Burna, Everest, and Skenta. Lady Bellford, Diamont respectively, and Brofent showed intermediate disease severity. Flora cultivar exhibited the least degree of scab symptoms. The role of certain potato tubers constituents in the physiology of disease susceptibility was investigated (sugar contents, pectin substances and calcium contents), Lady Bellford cultivar contained the highest concentration of total sugar followed by Flora, Burna, and Everest but Skenta, Lady Rosette respectively and Diamont were approximately had equal in total sugar contents, while, Brofent cultivar contained the lowest content of total sugar. Skenta cultivar contained the highest concentration of pectin substances and calcium contents followed by Flora and Lady Bellford finally Burna cultivars respectively.


2000 ◽  
Vol 78 (3) ◽  
pp. 374-380 ◽  
Author(s):  
Claudia Goyer ◽  
Pierre-Mathieu Charest ◽  
Vicky Toussaint ◽  
Carole Beaulieu

The cytological and ultrastructural modifications induced by thaxtomin A, a phytotoxin produced by Streptomyces scabies, were analyzed on mature field-grown potato tuber tissues. In tissue sampled during the first 12 h after treatment with thaxtomin A, the plasmalemma of parenchyma cells was detached from the cell wall in several places. However, the plasmalemma did not appear ruptured. The intercellular spaces between the retracted plasmalemma and the cell wall often contained fibrillar material. After a longer period of time, cells from tissues treated with thaxtomin A showed significant disorganization, such as detachment and invagination of the plasmalemma, the presence of a fibrillar-like material in the cytoplasm, and electron-dense material associated with moribund cellular features.Key words: common scab, potato, phytotoxin, Solanum tuberosum.


2004 ◽  
Vol 50 (2) ◽  
pp. 121-126 ◽  
Author(s):  
George Lazarovits ◽  
Jackie Hill ◽  
Russell R King ◽  
Larry A Calhoun

Of several hundred microorganisms randomly selected from the environment, only a fungal isolate identified as Aspergillus niger van Tiegham var. niger was found to transform the phytotoxin thaxtomin A to much less toxic metabolites. The rate and extent of transformation of thaxtomin A was tested under a variety of conditions, including different growth media, biomass concentrations, incubation periods, and shaker speeds. Under optimum conditions the fungus converted thaxtomin A into two major and five minor metabolites. The two major metabolites and three of the five minor metabolites were fully characterized by a combination of mass spectral and nuclear magnetic resonance techniques. When assayed on aseptically produced mini-tubers, the major metabolites proved to be much less phytotoxic than thaxtomin A.Key words: Aspergillus niger van Tiegham var. niger, biotransformation, common scab, phytotoxins, Streptomyces scabies, thaxtomin A.


2010 ◽  
Vol 100 (1) ◽  
pp. 91-96 ◽  
Author(s):  
Sylvain Lerat ◽  
Anne-Marie Simao-Beaunoir ◽  
Run Wu ◽  
Nathalie Beaudoin ◽  
Carole Beaulieu

Streptomyces scabies is a gram-positive soil bacterium recognized as the main causal agent of common scab. Pathogenicity in Streptomyces spp. depends on their capacity to synthesize phytotoxins called thaxtomins. Genes involved in biosynthesis of these secondary metabolites are known to be induced by cellobiose, a plant disaccharide. However, growth of S. scabies in a minimal medium containing cellobiose as a carbon source is very poor and only generates traces of thaxtomins. The effect of suberin, a lipid plant polymer, on thaxtomin A biosynthesis and the expression of genes involved in its biosynthetic pathway was analyzed. S. scabies was grown in a starch-containing minimal medium supplemented with cellobiose (0.5%), suberin (0.1%), or both. The presence of both cellobiose and suberin doubled bacterial growth and triggered thaxtomin A production, which correlated with the upregulation (up to 342-fold) of genes involved in thaxtomins synthesis. The addition of either suberin or cellobiose alone did not affect these parameters. Suberin appeared to stimulate the onset of secondary metabolism, which is a prerequisite to the production of molecules such as thaxtomin A, while cellobiose induced the biosynthesis of this secondary metabolite.


1985 ◽  
Vol 54 (03) ◽  
pp. 612-616 ◽  
Author(s):  
A J Carter ◽  
S Heptinstall

SummaryThe platelet aggregation that occurred in whole blood in response to several aggregating agents (collagen, arachidonic acid, adenosine diphosphate, adrenaline and thrombin) was measured using an Ultra-Flo 100 Whole Blood Platelet Counter. The amounts of thromboxane B2 produced were measured by radioimmunoassay. The effects of various inhibitors of thromboxane synthesis and the effects of apyrase, an enzyme that destroys adenosine diphosphate, were determined.Platelet aggregation was always accompanied by the production of thromboxane B2, and the amounts produced depended on the nature and concentration of the aggregating agent used. The various inhibitors of thromboxane synthesis - aspirin and flurbiprofen (cyclo-oxygenase inhibitors), BW755C (a cyclo-oxygenase and lipoxygenase inhibitor) and dazoxiben (a selective thromboxane synthase inhibitor) - did not markedly inhibit aggregation. Results obtained using apyrase showed that adenosine diphosphate contributed to the aggregation process, and that its role must be acknowledged when devising means of inhibiting platelet aggregation in vivo.


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