Stringent control of ribonucleic acid synthesis in <i>Bacillus subtilis</i> treated with granaticin

Ogilvie, Adaling; Wiebauer, Karin; Kersten, W.

doi:10.1042/bj1520517

Cited by 30 publications

(20 citation statements)

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“…Other antibiotics that are known to induce the accumulation of ppGpp include granaticin (33,34), chloroquinone (32,35), and certain polypeptide antibiotics (11). Chloroquinone and granaticin induce the stringent response by specifically creating a leucine auxotrophy in treated cells (33,35 5) and P. aeruginosa, which have previously not been reported to modulate growth through ppGpp, respond to ES treatment by accumulating high levels of ppGpp.…”

Section: Resultsmentioning

confidence: 99%

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The role of guanosine-3',5'-bis-pyrophosphate in mediating antimicrobial activity of the antibiotic 3,5-dihydroxy-4-ethyl-trans-stilbene

Sundar

Chang

1992

Antimicrob Agents Chemother

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The mode of action of 3,5-dihydroxy-4-ethyl-trans-stilbene (ES), an antibiotic produced by Xenorhabdus luminescens symbiotically associated with an entomopathogenic nematode, was investigated. ES was active against gram-positive and a number of gram-negative bacteria. In susceptible bacteria this antibiotic caused the inhibition of total RNA synthesis and, to a lesser extent, protein synthesis. At or above MICs, ES triggered a substantial accumulation of an intracellular regulatory compound, guanosine-3',5'-bis-pyrophosphate (ppGpp). This response was also noticed in species of bacteria which have previously not been shown to use ppGpp as a regulatory molecule. The involvement of ppGpp in antibiotic action was confirmed by using an isogenic stringent and a relaxed pair of Escherichia coli strains. The fact that the accumulation of ppGpp was correlated with the susceptibility of various gram-positive and gram-negative bacteria to ES suggests that this nucleotide is involved in the regulation of RNA synthesis and growth in all these microorganisms. Thus, inhibition of RNA synthesis via an increase in ppGpp concentrations may represent a mechanism that is prevalent among most bacteria and one that could be exploited for achieving a rapid inhibition of bacterial growth.

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Section: Resultsmentioning

confidence: 99%

“…To date, there are only a limited number of antibiotics which are known to cause bacterial growth inhibition largely by provoking the accumulation of ppGpp (11,34,35,39). This mode of antibiotic activity has obvious advantages over some others, since high levels of ppGpp lead to an almost immediate and severe inhibition of bacterial growth.…”

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confidence: 99%

The role of guanosine-3',5'-bis-pyrophosphate in mediating antimicrobial activity of the antibiotic 3,5-dihydroxy-4-ethyl-trans-stilbene

Sundar

Chang

1992

Antimicrob Agents Chemother

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“…S. thermoviolaceus is isolated readily from horse manure (Desai & Dhala, 1967) and granaticin has been shown to inhibit RNA synthesis by interference with leucyl-tRNA synthetase in Gram-positive bacteria, notably Bacillus spp. (Ogilvie et al, 1975;Weiser et al, 1977). It could be postulated therefore that if granaticin were synthesized in the environment it would confer a selective advantage for the survival and proliferation of S. thermoviolaceus over facultatively thermophilic Bacillus spp.…”

Section: Discussionmentioning

confidence: 99%

The Effects of Temperature on Growth and Production of the Antibiotic Granaticin by a Thermotolerant Streptomycete

James

Edwards

1989

Microbiology

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The synthesis of granaticin, a polyketide-derived antibiotic synthesized as a secondary metabolite by Streptomyces thermoviolaceus strain NCIB 10076, was studied at different growth temperatures. Quantitative measurements of the antibiotic made during batch fermentations showed that the yield was greatest at 45 "C, whereas the rate of synthesis was most rapid at 37 "C. The timing of the appearance of granaticin in culture could not be assigned to any particular phase of growth or to de-repression due to depletion of any particular nutrient. However, at all temperatures, appearance of the antibiotic coincided with a rise in ammoniacal nitrogen presumably due to deamination of glutamate, the carbon source for growth. We have previously shown that production of the antibiotic is pH sensitive and that some carbon sources result in higher titres than others. This paper examines the effect of temperature on the physiology of growth and on antibiotic production in more detail under conditions that also allow an exact measurement of granaticin yield. I N T R O D U C T I O NTaxonomic studies have revealed that many Streptomyces are able to grow at 45 "C (Williams et al., 1983). However until recently there were relatively few reports concerning the ability of species from this group to grow at temperatures in excess of 50 "C. Goodfellow et al. (1987) surveyed 50 thermophilic streptomycetes from a range of habitats which they were able to assign to a number of clusters in a numerical phenetic study that identified some features of their physiology and metabolic versatility. Such work is valuable in view of the commercial advantages of thermophilic species. These include faster reaction times and reduced cooling costs for large fermentations which make the thermophilic streptomycetes potentially useful vehicles for antibiotic production at high temperatures. Streptomyces thermoviolaceus is a particularly useful model system for such studies because it grows over a temperature range of around 25 to 58 "C (Edwards & Ball, 1987) and produces granaticin, a pigmented and pH sensitive antibiotic (Maehr et al., 1979) which is synthesized via the polyketide pathway (Arnone et al., 1979; Snipes et al., 1979). Snipes et al. (1979), using 13C-labelled acetate and glucose, showed that granaticin is produced by mixed biogenesis from eight acetate units and one dideoxyglucose moiety. This agrees with other radiolabelling work that showed polyketide antibiotics to be acetate derived (Floss et al., 1985). Using an lSO2 atmosphere, Floss et al. (1985) also demonstrated that no molecular oxygen was incorporated into the molecule, indicating a direct cyclization of the polyacetyl chain rather than a classical hydroxylation using molecular oxygen, followed by a dehydration to the lactone. METHODSOrganism and culture conditions. Streptomyces thermoviolaceus subsp. thermoviolaceus NCIB 10076 was maintained on complex solid medium that contained (g 1-l): glucose, 4; malt extract, 10; yeast extract, 4; and after adjusting to pH 7.2, agar, 20....

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“…Subsequently (stage 2), the amino acid moiety is transferred to its cognate tRNA and the resulting aminoacyl-tRNA acts as a substrate for polypeptide synthesis, which occurs on the ribosome (49). Inhibition of either one of these enzymatic stages leads to the accumulation of uncharged tRNA molecules, which bind to ribosomes, causing the interruption of polypeptide chain elongation (20,21,66,90). Induction of the stringent response by relA then occurs (20).…”

Section: Aminoacyl-trna Synthetases As Novel Antibacterial Targetsmentioning

confidence: 99%

Prospects for Aminoacyl-tRNA Synthetase Inhibitors as New Antimicrobial Agents

Hurdle

O’Neill

Chopra

2005

Antimicrob Agents Chemother

188

172

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Stringent control of ribonucleic acid synthesis in Bacillus subtilis treated with granaticin

Cited by 30 publications

References 20 publications

The role of guanosine-3',5'-bis-pyrophosphate in mediating antimicrobial activity of the antibiotic 3,5-dihydroxy-4-ethyl-trans-stilbene

The role of guanosine-3',5'-bis-pyrophosphate in mediating antimicrobial activity of the antibiotic 3,5-dihydroxy-4-ethyl-trans-stilbene

The Effects of Temperature on Growth and Production of the Antibiotic Granaticin by a Thermotolerant Streptomycete

Prospects for Aminoacyl-tRNA Synthetase Inhibitors as New Antimicrobial Agents

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