A limited concentration range of diaphorin, a polyketide produced by a bacterial symbiont of the Asian citrus psyllid, promotes thein vitrogene expression with bacterial ribosomes

Abstract

Diaphorin is a polyketide produced by “CandidatusProfftella armatura” (Gammaproteobacteria:Burkholderiales), an obligate symbiont of a devastating agricultural pest, the Asian citrus psyllidDiaphorina citri(Hemiptera: Psyllidae). Physiological concentrations of diaphorin, whichD. citricontains at levels as high as 2–20 mM, are inhibitory to various eukaryotes andBacillus subtilis(Firmicutes:Bacilli) but promote the growth and metabolic activity ofEscherichia coli(Gammaproteobacteria:Enterobacterales). Our previous study demonstrated that five-millimolar diaphorin, which exhibits significant inhibitory and promoting effects on culturedB. subtilisandE. coli, respectively, inhibitsin vitrogene expression utilizing purifiedB. subtilisandE. coliribosomes. This suggested that the adverse effects of diaphorin onB. subtilisare partly due to its influence on gene expression. However, the result appeared inconsistent with the positive effects onE. coli. Moreover, the diaphorin concentration in bacterial cells, where genes are expressedin vivo, may be lower than in culture media. Therefore, the present study analyzed the effects of 50 and 500 μM of diaphorin on bacterial gene expression using the same analytical method. The result revealed that this concentration range of diaphorin, in contrast to five-millimolar diaphorin, promotes thein vitrotranslation with theB. subtilisandE. coliribosomes, suggesting that the positive effects of diaphorin onE. coliare due to its direct effects on translation. This study demonstrated for the first time that a pederin-type compound promotes gene expression, establishing a basis for utilizing its potential in pest management and industrial applications.ImportanceThis study revealed that a limited concentration range of diaphorin, a secondary metabolite produced by a bacterial symbiont of an agricultural pest, promotes cell-free gene expression utilizing substrates and proteins purified from bacteria. The unique property of diaphorin, which is inhibitory to various eukaryotes andBacillus subtilisbut promotes the growth and metabolic activity ofEscherichia coli, may affect the microbial flora of the pest insect, potentially influencing the transmission of devastating plant pathogens. Moreover, the activity may be exploited to improve the efficacy of industrial production byE. coli, which is often used to produce various important materials, including pharmaceuticals, enzymes, amino acids, and biofuels. This study elucidated a part of the mechanism by which the unique activity of diaphorin is expressed, constructing a foundation for applying the unique property to pest management and industrial use.