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Nitrogen Sources Inhibit Biofilm Formation by Xanthomonas oryzae pv. oryzae

  • Ham, Youngseok (Department of Forest Products and Biotechnology, College of Science and Technology, Kookmin University) ;
  • Kim, Tae-Jong (Department of Forest Products and Biotechnology, College of Science and Technology, Kookmin University)
  • Received : 2018.08.16
  • Accepted : 2018.10.09
  • Published : 2018.12.28

Abstract

Xanthomonas oryzae pv. oryzae (Xoo) causes bacterial blight, which results in severe economic damage to rice farms. Xoo produces biofilms for pathogenesis and survival both inside and outside the host. Biofilms, which are important virulence factors, play a key role in causing the symptoms of Xoo infection. In the present study, we investigated the nutritional conditions for biofilm formation by Xoo. Although Xoo biofilm formation may be initiated by interactions with the host, Xoo biofilm cannot mature without the support of favorable nutritional conditions. Nitrogen sources inhibited Xoo biofilm formation by overwhelming the positive effect that cell growth has on it. However, limited nutrients with low amino acid concentration supported biofilm formation by Xoo in the xylem sap rather than in the phloem sap of rice.

Keywords

References

  1. Swings J, Van Den Mooter M, Vauterin L, Hoste B, Gillis M, Mew TW, et al. 1990. Reclassification of the causal agents of bacterial blight (Xanthomonas campestris pv. oryzae) and bacterial leaf streak (Xanthomonas campestris pv. Oryzicola) of rice as pathovars of Xanthomonas oryzae (ex ishiyama 1922) sp. Nov., nom. Rev. Int. J. Syst. Bacteriol. 40: 309-311. https://doi.org/10.1099/00207713-40-3-309
  2. Adhikari TB, Mew TW, Teng PS. 1994. Progress of bacterial blight on rice cultivars carrying different xa genes for resistance in the field. Plant Dis. 78: 73-77. https://doi.org/10.1094/PD-78-0073
  3. Durgapal JC. 1985. Self-sown plants from bacterial blightinfected rice seeds - a possible source of primary infection in northwest india. Curr. Sci. India 54: 1283-1284.
  4. Devadath S, Dath AP. 1985. Infected chaff as a source of inoculum of Xanthomonas campestris pv. oryzae to the rice crop. J. Plant Dis. Protect. 92: 485-488.
  5. Hsieh SPY, Buddenhagen IW, Kauffman HE. 1974. An improved method for detecting the presence of Xanthomonas oryzae in rice seed. Phytopathology 64: 273-274. https://doi.org/10.1094/Phyto-64-273
  6. Murty VST, Devadath S. 1984. Role of seed in survival and transmission of Xanthomonas campestris pv. oryzae causing bacterial blight of rice. J. Phytopathol. 110: 15-19. https://doi.org/10.1111/j.1439-0434.1984.tb00735.x
  7. Mew TW, Unnamalai N, Baraoidan MR. 1989. Presented at the Bacterial Blight of Rice, Proceedings of the International Workshop on Bacterial Blight of Rice, Manila, Philippines, March 14-18, 1988.
  8. Singh RN. 1971. Perpetuation of bacterial blight disease of paddy and preservation of its incitant. Ii. Survival of Xanthomonas oryzae in soil. Indian Phytopathol. 24: 153-154.
  9. Murty VST, Devadath S. 1982. Survival of Xanthomonas campestris pv. oryzae in different soils. Indian Phytopathol. 35: 32-38.
  10. Stoodley P, Sauer K, Davies DG, Costerton JW. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56: 187-209. https://doi.org/10.1146/annurev.micro.56.012302.160705
  11. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15: 167-193. https://doi.org/10.1128/CMR.15.2.167-193.2002
  12. Valerie NDG, Natalie V, Maarten F, Cyrielle IK, Aline MV, Serge B, et al. 2009. Novel persistence genes in Pseudomonas aeruginosa identified by high-throughput screening. FEMS Microbiol. Lett. 297: 73-79. https://doi.org/10.1111/j.1574-6968.2009.01657.x
  13. Souza AA, Takita MA, Coletta-Filho HD, Caldana C, Yanai GM, Muto NH, et al. 2004. Gene expression profile of the plant pathogen Xylella fastidiosa during biofilm formation in vitro. FEMS Microbiol. Lett. 237: 341-353.
  14. Lim SH, So BH, Wang JC, Song ES, Park YJ, Lee BM, et al. 2008. Functional analysis of pilq gene in Xanthomanas oryzae pv. oryzae, bacterial blight pathogen of rice. J. Microbiol. 46: 214-220. https://doi.org/10.1007/s12275-007-0173-9
  15. Pradhan BB, Ranjan M, Chatterjee S. 2012. Xadm, a novel adhesin of Xanthomonas oryzae pv. oryzae, exhibits similarity to rhs family proteins and is required for optimum attachment, biofilm formation, and virulence. Mol. Plant Microbe In. 25: 1157-1170. https://doi.org/10.1094/MPMI-02-12-0049-R
  16. Su J, Zou X, Huang L, Bai T, Liu S, Yuan M, et al. 2016. DgcA, a diguanylate cyclase from Xanthomonas oryzae pv. oryzae regulates bacterial pathogenicity on rice. Sci. Rep.-UK 6: 25978. https://doi.org/10.1038/srep25978
  17. Crutis LC. 1943. Deleterious effects of guttated fluid on foliage. Am. J. Bot. 30: 778-781. https://doi.org/10.1002/j.1537-2197.1943.tb10330.x
  18. Ou SH. 1985. Rice disease. Commonwealth Agricultural Bureau, Kew, Surrey, England.
  19. Noda T, Kaku H. 1999. Growth of Xanthomonas oryzae pv. oryzae in planta and in guttation fluid of rice. Ann. Phytopathol. Soc. Jpn. 65: 9-14. https://doi.org/10.3186/jjphytopath.65.9
  20. Grewal RK, Gupta S, Das S. 2012. Xanthomonas oryzae pv oryzae triggers immediate transcriptomic modulations in rice. BMC Genomics 13: 49. https://doi.org/10.1186/1471-2164-13-49
  21. Hilaire E, Young SA, Willard LH, McGee JD, Sweat T, Chittoor JM, et al. 2001. Vascular defense responses in rice: Peroxidase accumulation in xylem parenchyma cells and xylem wall thickening. Mol. Plant Microbe. Interact. 14: 1411-1419. https://doi.org/10.1094/MPMI.2001.14.12.1411
  22. Young SA, Guo A, Guikema JA, White FF, Leach JE. 1995. Rice cationic peroxidase accumulates in xylem vessels during incompatible interactions with Xanthomonas oryzae pv oryzae. Plant Physiol. 107: 1333-1341. https://doi.org/10.1104/pp.107.4.1333
  23. Han SW, Park CJ, Lee SW, Ronald P. 2008. An efficient method for visualization and growth of fluorescent Xanthomonas oryzae pv. oryzae in planta. BMC Microbiol. 8: 164. https://doi.org/10.1186/1471-2180-8-164
  24. Mew TW, Alvarez AM, Leach JE, Swings J. 1993. Focus on bacterial blight of rice. Plant Dis. 77: 5-12. https://doi.org/10.1094/PD-77-0005
  25. Lee BM, Park YJ, Park DS, Kang HW, Kim JG, Song ES, et al. 2005. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucl. Acids Res. 33: 577-586. https://doi.org/10.1093/nar/gki206
  26. Kim H S, Park HJ, Heu S, Jung J. 2004. Molecular a nd functional characterization of a unique sucrose hydrolase from Xanthomonas axonopodis pv. Glycines. J. Bacteriol. 186: 411-418. https://doi.org/10.1128/JB.186.2.411-418.2004
  27. Shaw JJ, Dane F, Geiger D, Kloepper JW. 1992. Use of bioluminescence for detection of genetically engineered microorganisms released into the environment. Appl. Environ. Microbiol. 58: 267-273.
  28. Myung IS, Cho Y, Lee YH, Kwon HM. 2001. Phage typing and lysotype distribution of Xanthomonas axonopodis pv. Citri, the causal agent of citrus bacterial canker in Korea. Plant Pathol. J. 17: 336-341.
  29. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
  30. Tsuge S, Furutani A, Fukunaka R, Oku T, Tsuno K, Ochiai H, et al. 2002. Expression of Xanthomonas oryzae pv. oryzae hrp genes in XOM2, a novel synthetic medium. J. Gen. Plant Pathol. 68: 363-371. https://doi.org/10.1007/PL00013104
  31. Ryan RP, Fouhy Y, Lucey JF, Jiang B-L, He Y-Q, Feng J-X, et al. 2007. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol. Microbiol. 63: 429-442. https://doi.org/10.1111/j.1365-2958.2006.05531.x
  32. Bailey KJ, Leegood RC. 2016. Nitrogen recycling from the xylem in rice leaves: Dependence upon metabolism and associated changes in xylem hydraulics. J. Exp. Bot. 67: 2901-2911. https://doi.org/10.1093/jxb/erw132
  33. Fukumorita T, Chino M. 1982. Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol. 23: 273-283.
  34. Kim TJ, Young BM, Young GM. 2008. Effect of flagellar mutations on Yersinia enterocolitica biofilm formation. Appl. Environ. Microbiol. 74: 5466-5474. https://doi.org/10.1128/AEM.00222-08
  35. Sharma S, Lavender S, Woo J, Guo L, Shi W, Kilpatrick- Liverman L, et al. 2014. Nanoscale characterization of effect of L-arginine on Streptococcus mutans biofilm adhesion by atomic force microscopy. Microbiology 160: 1466-1473. https://doi.org/10.1099/mic.0.075267-0
  36. Jakubovics NS, Robinson JC, Samarian DS, Kolderman E, Yassin SA, Bettampadi D, et al. 2015. Critical roles of arginine in growth and biofilm development by Streptococcus gordonii. Mol. Microbiol. 97: 281-300. https://doi.org/10.1111/mmi.13023
  37. Nascimento MM, Browngardt C, Xiaohui X, Klepac-Ceraj V, Paster BJ, Burne RA. 2014. The effect of arginine on oral biofilm communities. Mol. Oral Microbiol. 29: 45-54. https://doi.org/10.1111/omi.12044
  38. Tada A, Nakayama-Imaohji H, Yamasaki H, Hasibul K, Yoneda S, Uchida K, et al. 2016. Cleansing effect of acidic L-arginine on human oral biofilm. BMC Oral Health 16: 40. https://doi.org/10.1186/s12903-016-0194-z
  39. John G, Becker J, Schwarz F. 2016. Effectivity of air-abrasive powder based on glycine and tricalcium phosphate in removal of initial biofilm on titanium and zirconium oxide surfaces in an ex vivo model. Clin. Oral Invest. 20: 711-719. https://doi.org/10.1007/s00784-015-1571-8
  40. Gnanadhas DP, Elango M, Datey A, Chakravortty D. 2015. Chronic lung infection by Pseudomonas aeruginosa biofilm is cured by L-methionine in combination with antibiotic therapy. Sci. Rep.-UK 5: 16043. https://doi.org/10.1038/srep16043
  41. Brandenburg KS, Rodriguez KJ, McAnulty JF, Murphy CJ, Abbott NL, Schurr MJ, et al. 2013. Tryptophan inhibits biofilm formation by Pseudomonas aeruginosa. Antimicrob. Agents Ch. 57: 1921-1925. https://doi.org/10.1128/AAC.00007-13
  42. Schlag S, Nerz C, Birkenstock TA, Altenberend F, Gotz F. 2007. Inhibition of staphylococcal biofilm formation by nitrite. J. Bacteriol. 189: 7911-7919. https://doi.org/10.1128/JB.00598-07
  43. Meng Y, Li Y, Galvani CD, Hao G, Turner JN, Burr TJ, et al. 2005. Upstream migration of Xylella fastidiosa via pilusdriven twitching motility. J. Bacteriol. 187: 5560-5567. https://doi.org/10.1128/JB.187.16.5560-5567.2005
  44. Vu B, Chen M, Crawford R, Ivanova E. 2009. Bacterial extracellular polysaccharides involved in biofilm formation. Molecules. 14: 2535-2554. https://doi.org/10.3390/molecules14072535
  45. Dharmapuri S, Sonti RV. 1999. A transposon insertion in the gumg homologue of Xanthomonas oryzae pv. oryzae causes loss of extracellular polysaccharide production and virulence. FEMS Microbiol. Lett. 179: 53-59. https://doi.org/10.1111/j.1574-6968.1999.tb08707.x
  46. Singh VB, Kumar A, Isaac Kirubakaran S, Ayyadurai N, Sunish Kumar R, Sakthivel N. 2006. Comparison of exopolysaccharides produced by Xanthomonas oryzae pv. oryzae strains, BXO1 and BXO8 that show varying degrees of virulence in rice (Oryza sativa L.). J. Phytopathol. 154: 410-413. https://doi.org/10.1111/j.1439-0434.2006.01114.x
  47. Singh A, Gupta R, Tandon S, Pandey R. 2017. Thyme oil reduces biofilm formation and impairs virulence of Xanthomonas oryzae. Front. Microbiol. 8: 1074. https://doi.org/10.3389/fmicb.2017.01074
  48. Doi R, Ranamukhaarachchi SL. 2009. Correlations between soil microbial and physicochemical variations in a rice paddy: implications for assessing soil health. J. Biosci. 34: 969-976. https://doi.org/10.1007/s12038-009-0111-6