Skip to main content

Advertisement

Log in

Antibacterial activity and mechanism of ThDP analogs against rice brown stripe pathogen Acidovorax avenae subsp. avenae RS-1

  • Original Article
  • Published:
Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Thiamin diphosphate (ThDP) analogs have been designed and synthesized based on the ThDP binding site of the pyruvate dehydrogenase multienzyme complex E1 of Escherichia coli. This study investigated the effect of 66 novel ThDP analogs on rice bacterial brown stripe pathogen Acidovorax avenae subsp. avenae strain RS-1. Results indicated that three of the 66 ThDP analogs (designated as 20, 21 and 53) significantly inhibited the in vitro growth of strain RS-1. However, no obvious cell lysis and destruction was found for this rice pathogenic bacterium, which were supported by morphological evidence of transmission electron microscope. In contrast, the three ThDP analogs significantly reduced biofilm formation and the activity of the pyruvate dehydrogenase of strain RS-1. Furthermore, the differential expression of ThDP target gene and 20 secretion system related genes were revealed by using quantitative real-time PCR. Among these, the expressions of ThDP target gene and VgrG-5 under the treatment of ThDP 20 were strongly induced compared to the control, which indicated that the antibacterial mechanism of ThDP analogs may be mainly due to the changed expression of ThDP target gene and secretion system related genes rather than causing damage to cell membrane. Taken together, the application of synthesized ThDP analogs might be a tractable strategy to overcome the pathogen of rice bacterial brown stripe.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arjunan P, Chandrasekhar K, Sax M, Brunskill A, Nemeria N, Jordan F, Furey W (2004) Structural determinants of enzyme binding affinity: the E1 component of pyruvate dehydrogenase from Escherichia coli in complex with the inhibitor thiamin thiazolone diphosphate. Biochemistry 43:2405–2411

    Article  CAS  PubMed  Google Scholar 

  • Aschtgen MS, Bernard CS, De BS, Lloubès R, Cascales E (2008) SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J Bacteriol 190:7523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baillie AC, Wright K, Wright BJ, Earnshaw CG (1988) Inhibitors of pyruvate dehydrogenase as herbicides. Pestic Biochem Physiol 30:103–112

    Article  CAS  Google Scholar 

  • Behal RH, Buxton DB, Robertson JG, Olson MS (1993) Regulation of thePyruvate dehydrogenase multienzyme complex. Annu Rev Nutr 13:497–520

    Article  CAS  PubMed  Google Scholar 

  • Birkenstock T, Liebeke M, Winstel V, Krismer B, Gekeler C, Niemiec MJ, Bisswanger H, Lalk M, Peschel A (2012) Exometabolome analysis identifies pyruvate dehydrogenase as a target for the antibiotic triphenylbismuthdichloride in multiresistant bacterial pathogens. J Biol Chem 287:2887–2895

    Article  CAS  PubMed  Google Scholar 

  • Chen CZ, Cooper SL (2002) Interactions between dendrimer biocides and bacterial membranes. Biomaterials 23:3359–3368

    Article  CAS  PubMed  Google Scholar 

  • Cui Z, Jin G, Li B, Kakar KU, Ojaghian MR, Wang Y, Xie G, Sun G (2015) Gene expression of type VI secretion system associated with environmental survival in Acidovorax avenae subsp. avenae by principle component analysis. Int J Mol Sci 16:22008–22026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies DG, Chakrabarty AM, Geesey GG (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl Environ Microbiol 59:1181–1186

    CAS  PubMed  PubMed Central  Google Scholar 

  • De BD, Stoodley P, Lewandowski Z (1994) Liquid flow in heterogeneous biofilms. Biotechnol Bioeng 44:636–641

    Article  Google Scholar 

  • Dong Q, Luo J, Qiu W, Cai L, Anjum SI, Li B, Hou M, Xie G, Sun G (2016) Inhibitory effect of Camptothecin against Rice bacterial Brown stripe pathogen Acidovorax avenae subsp. avenae RS-2. Molecules 21:978

    Article  CAS  PubMed Central  Google Scholar 

  • Fouque F, Brivet MA, Vequaud C, Marsac C, Zabot MT, Benelli C (2003) Differential effect of DCA treatment on the pyruvate dehydrogenase complex in patients with severe PDHC deficiency. Pediatr Res 53:793–799

    Article  CAS  PubMed  Google Scholar 

  • He JB, Feng LL, Li J, Tao RJ, Ren YL, Wan J, He HW (2014) Design, synthesis and molecular modeling of novel N-acylhydrazone derivatives as pyruvate dehydrogenase complex E1 inhibitors. Bioorg Med Chem 22:89–94

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim M, Shi Y, Qiu H, Li B, Jabeen A, Li L, Liu H, Kube M, Xie G, Wang Y (2012) Differential expression of in vivo and in vitro protein profile of outer membrane of Acidovorax avenae subsp. avenae. Plos One 7:e49657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jani AJ, Cotter PA (2010) Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 8:2–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kakar KU, Nawaz Z, Cui Z, Almoneafy AA, Zhu B, Xie GL (2014) Characterizing the mode of action of Brevibacillus laterosporus B4 for control of bacterial brown strip of rice caused by Acidovorax avenae subsp. avenae RS-1. World Journal of Microbiology & Biotechnology 30:469–478

    Article  CAS  Google Scholar 

  • Li B, Wang X, Chen RX, Huangfu WG, Xie GL (2008) Antibacterial activity of chitosan solution against Xanthomonas pathogenic bacteria isolated from Euphorbia pulcherrima. Carbohydr Polym 72:287–292

    Article  CAS  Google Scholar 

  • Li B, Liu B, Yu R, Tao Z, Wang Y, Xie G, Li H, Sun G (2011) Bacterial brown stripe of rice in soil-less culture system caused by Acidovorax avenae subsp. avenae in China. J Gen Plant Pathol 77:64–67

    Article  Google Scholar 

  • Li B, Shi Y, Shan C, Zhou Q, Ibrahim M, Wang Y, Wu G, Li H, Xie G, Sun G (2013) Effect of chitosan solution on the inhibition of Acidovorax citrulli causing bacterial fruit blotch of watermelon. J Sci Food Agric 93:1010–1015

    Article  CAS  PubMed  Google Scholar 

  • Li B, Ge M, Zhang Y, Wang L, Ibrahim M, Wang Y, Sun G, Chen G (2016) New insights into virulence mechanisms of rice pathogen Acidovorax avenae subsp. avenae strain RS-1 following exposure to ß-lactam antibiotics. Scientific Reports 6:2241

    Google Scholar 

  • Liu H, Tian WX, Ibrahim M, Li B, Zhang GQ, Zhu B, Xie GL (2012) Characterization of pilP, a gene required for twitching motility, pathogenicity, and biofilm formation of Acidovorax avenae subsp. avenae RS-1. Eur J Plant Pathol 134:551–560

    Article  CAS  Google Scholar 

  • Lou MM, Zhu B, Muhammad I, Li B, Xie GL, Wang YL, Li HY, Sun GC (2011) Antibacterial activity and mechanism of action of chitosan solutions against apricot fruit rot pathogen Burkholderia seminalis. Carbohydr Res 346:1294–1301

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Sprenger GA, Pohl M (2013) CC bond formation using ThDP-dependent lyases. Curr Opin Chem Biol 17:261–270

    Article  CAS  PubMed  Google Scholar 

  • Nemeria N, Yan Y, Zhang Z, Brown A, Arjunan P, Furey W, Guest J, Jordan F (2001) Inhibition of the Escherichia coli pyruvate dehydrogenase complex E1 subunit and its tyrosine 177 variants by thiamin 2-thiazolone and thiamin 2-thiothiazolone diphosphates. Evidence for reversible tight-binding inhibition. J Biol Chem 276:45969–45978

    Article  CAS  PubMed  Google Scholar 

  • Patel MS, Roche TE (1990) Molecular biology and biochemistry of pyruvate dehydrogenase complexes. FASEB J 4:3224–3233

    Article  CAS  PubMed  Google Scholar 

  • Peeters E, Nelis HJ, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods 72:157–165

    Article  CAS  PubMed  Google Scholar 

  • Pii Y, Astegno A, Peroni E, Zaccardelli M, Pandolfini T, Crimi M (2009) The Medicago truncatula N5 gene encoding a root-specific lipid transfer protein is required for the symbiotic interaction with Sinorhizobium meliloti. Mol Plant Microbe Interact 22:1577–1587

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, He J, Feng L, Liao X, Jin J, Li Y, Cao Y, Wan J, He H (2011) Structure-based rational design of novel hit compounds for pyruvate dehydrogenase multienzyme complex E1 components from Escherichia coli. Bioorg Med Chem 19:7501–7506

    Article  CAS  PubMed  Google Scholar 

  • Santiviago CA, Inés C, Jiménez JC, Blondel CJ (2009) Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10:354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz R, Reed LJ (1970) Regulation of the activity of the pyruvate dehydrogenase complex of Escherichia coli. Biochemistry 9:1434–1439

    Article  CAS  PubMed  Google Scholar 

  • Song WY, Kim HM, Hwang CY, Schaad NW (2004) Detection of Acidovorax avenae ssp. avenae in Rice seeds using BIO-PCR. J Phytopathol 152:667–676

    Article  CAS  Google Scholar 

  • Stacpoole PW (2012) The pyruvate dehydrogenase complex as a therapeutic target for age-related diseases. Aging Cell 11:371–377

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Zhou Q, Li B, Liu B (2012) Differentiation in MALDI-TOF MS and FTIR spectra between two closely related species Acidovorax oryzae and Acidovorax citrulli. BMC Microbiol 12:1–7

    Article  CAS  Google Scholar 

  • Weber B, Hasic M, Chen C, Wai S, Milton D (2010) Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environ Microbiol 11:3018–3028

    Article  CAS  Google Scholar 

  • Xie GL, Zhang GQ, Liu H, Lou MM, Tian WX, Li B, Zhou XP, Zhu B, Jin GL (2011) Genome sequence of the Rice-pathogenic bacterium Acidovorax avenae subsp. avenae RS-1. J Bacteriol 193:5013–5014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C, Li B, Ge M, Zhou K, Wang Y, Luo J, Ibrahim M, Xie G, Sun G (2014) Inhibitory effect and mode of action of chitosan solution against rice bacterial brown stripe pathogen Acidovorax avenae subsp. avenae RS-1. Carbohydr Res 391:48–54

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Science Foundation of China (31571971, 31371904, 21472062), Zhejiang Provincial Project (2017C02002), National Key Research and Development Program of China (2017YFD0201104), Shanghai Agricultural Basic Research Project (2014:7-3-1), the Fundamental Research Funds for the Central Universities, the Agricultural Ministry of China (nyhyzx 201303015), National Basic Research Program of China (No. 2010CB126100), Dabeinong Funds for Discipline Development and Talent Training in Zhejiang University, Key Subject Construction Program of Zhejiang for Modern Agricultural Biotechnology and Crop Disease Control (2010DS700124- KF1710), China Postdoctoral Science Foundation (Grant No. 2017 M612003).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Wen Qiu or Guo Chang Sun.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X.X., Qi, H.Y., Chen, J. et al. Antibacterial activity and mechanism of ThDP analogs against rice brown stripe pathogen Acidovorax avenae subsp. avenae RS-1. J Plant Pathol 101, 59–69 (2019). https://doi.org/10.1007/s42161-018-0137-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42161-018-0137-4

Keywords

Navigation