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A new function of the biocontrol bacterium Lysobacter enzymogenes LE16 in the mineralization of soil organic phosphorus

  • Danmei Chen
  • Jianguo Huang
  • Ling YuanEmail author
Regular Article
  • 60 Downloads

Abstract

Aims

To evaluate the functions of a new biocontrol bacterium, Lysobacter enzymogenes LE16, in the mineralization of soil organic phosphorus (P) and in the stimulation of plant P uptake and plant growth.

Methods

Liquid culture, soil incubation, and pot experiments were used to study phosphatase production, inorganic P release from lecithin and soil organic P compounds, and the P uptake and growth of lettuce seedlings induced by L. enzymogenes LE16.

Results

This bacterium hydrolyzed lecithin by the release of acid, neutral and alkaline phosphatases in culture solutions with a pH ranging from 4.0 to 10.0 at 12–36 °C. The hydrolysis reactions were unaffected by NH4+-N, NO3-N or urea at equal N concentrations but were promoted by low inorganic P. Bacterial inoculation significantly decreased the organic P but increased the water-soluble P and Olsen P in the soil. Compared to the use of chemical fertilizers alone, the P uptake, biomass, and economic yield of lettuce increased by 16.41%, 11.58%, and 11.30%, respectively, with an increase in soil Olsen P in the L. enzymogenes LE16 plus chemical fertilizer treatment.

Conclusions

Environmental adaptation and phosphatase production could be the mechanisms involved in soil P mineralization and plant pathogen suppression by L. enzymogenes LE16. This is the first demonstration of a new use of L. enzymogenes LE16 in agriculture beyond plant protection.

Keywords

Lysobacter enzymogenes Phosphatase Soil organic phosphorus Growth promotion 

Notes

Acknowledgments

This research work was financially supported by the Chongqing Scientific Innovation Project for Postgraduates (Project CYB17064), Chongqing Science and Technology Committee (cstc2018jscx-mszd0133 and cstc2017shms-xdny80084), and Zunyi Tobacco Company (ZY 2015-03 and ZY 2018-01).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human participants and/or animals

There is no research involving Human Participants and/or Animals in this article.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Ahuja A, Ghosh S, D’souza S (2007) Isolation of a starch utilizing, phosphate solubilizing fungus on buffered medium and its characterization. Bioresour Technol 98:3408–3411CrossRefGoogle Scholar
  2. Aledo JC, Jiménez-Riveres S, Tena M (2010) The effect of temperature on the enzyme-catalyzed reaction: insights from thermodynamics. J Chem Educ 87:296–298CrossRefGoogle Scholar
  3. Bakhshandeh E, Rahimian H, Pirdashti H, Nematzadeh GA (2014) Phosphate solubilization potential and modeling of stress tolerance of rhizobacteria from rice paddy soil in northern Iran. World J Microbiol Biotechnol 30:2437–2447CrossRefGoogle Scholar
  4. Borch K, Bouma T, Lynch J, Brown K (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431CrossRefGoogle Scholar
  5. Chen J, Moore W, Yuen GY, Kobayashi D, Caswell-Chen EP (2006) Influence of Lysobacter enzymogenes strain C3 on nematodes. J Nematol 38:233–239Google Scholar
  6. Christensen P, Cook F (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. Int J Syst Evol Microbiol 28:367–393Google Scholar
  7. Clarholm M, Skyllberg U, Rosling A (2015) Organic acid induced release of nutrients from metal-stabilized soil organic matter-the unbutton model. Soil Biol Biochem 84:168–176CrossRefGoogle Scholar
  8. Folman LB, Postma J, Veen J (2003a) Inability to find consistent bacterial biocontrol agents of Pythium aphanidermatum in cucumber using screens based on ecophysiological traits. Microb Ecol 45:72–87CrossRefGoogle Scholar
  9. Folman LB, Postma J, van Veen JA (2003b) Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1 T8, a powerful antagonist of fungal diseases of cucumber. Microbiol Res 158:107–115CrossRefGoogle Scholar
  10. Folman LB, De Klein M, Postma J, Van Veen J (2004) Production of antifungal compounds by Lysobacter enzymogenes isolate 3.1 T8 under different conditions in relation to its efficacy as a biocontrol agent of Pythium aphanidermatum in cucumber. Biol Control 31:145–154CrossRefGoogle Scholar
  11. Halder A, Mishra A, Chakrabarty P (1991) Solubilization of inorganic phosphates by Bradyrhizobium. Indian J Exp Biol 29:28–31Google Scholar
  12. He TX, Xie DT, Li ZL, Ni JP, Sun Q (2017) Ammonium stimulates nitrate reduction during simultaneous nitrification and denitrification process by Arthrobacter arilaitensis Y-10. Bioresour Technol 239:66–73CrossRefGoogle Scholar
  13. Hernández I (1996) Analysis of the expression of alkaline phosphatase activity as a measure of phosphorus status in the red alga Porphyra umbilicalis (L.) Kützing. Bot Mar 39:255–262CrossRefGoogle Scholar
  14. Huang JL, Su ZC, Xu Y (2005) The evolution of microbial phosphonate degradative pathways. J Mol Evol 61:682–690CrossRefGoogle Scholar
  15. Islam MT (2011) Potentials for biological control of plant diseases by Lysobacter spp., with special reference to strain SB-K88. In: Maheshwari D (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin, HeidelbergGoogle Scholar
  16. Ji GH (2011) Advances in the studies on Lysobacter sp. and their effects on biological control of plant diseases. J Yunnan Agric Univ 26:124–130Google Scholar
  17. Ji GH, Wei LF, He YQ, Wu YP, Bai XH (2008) Biological control of rice bacterial blight by Lysobacter antibioticus strain 13-1. Biol Control 45:288–296CrossRefGoogle Scholar
  18. Jochum C, Osborne L, Yuen GY (2006) Fusarium head blight biological control with Lysobacter enzymogenes strain C3. Biol Control 39:336–344CrossRefGoogle Scholar
  19. Katz AM (1982) Membrane-derived lipids and the pathogenesis of ischemic myocardial damage. J Mol Cell Cardiol 14:627–632CrossRefGoogle Scholar
  20. Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture-a review. Agron Sustain Dev 27:29–43CrossRefGoogle Scholar
  21. Kilic-Ekici O, Yuen GY (2004) Comparison of strains of Lysobacter enzymogenes and PGPR for induction of resistance against Bipolaris sorokiniana in tall fescue. Biol Control 30:446–455CrossRefGoogle Scholar
  22. Kleinman PJ, Sharpley AN (2003) Effect of broadcast manure on runoff phosphorus concentrations over successive rainfall events. J Environ Qual 32:1072–1081CrossRefGoogle Scholar
  23. Li S, Jochum C, Yu F, Zaleta-Rivera K, Du L, Harris SD, Yuen GY (2008) An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. Phytopathology 98:695–701CrossRefGoogle Scholar
  24. Li P, Liu WH, Gao KS (2013) Effects of temperature, pH, and UV radiation on alkaline phosphatase activity in the terrestrial cyanobacterium Nostoc flagelliforme. J Appl Phycol 25:1031–1038CrossRefGoogle Scholar
  25. Li B, Boiarkina I, Young B, Yu W, Singhai N (2018) Prediction of future phosphate rock: a demand based model. J Environ Inf 31:41–53Google Scholar
  26. Menezes-Blackburn D, Jorquera MA, Greiner R, Gianfreda L, de la Luz Mora M (2013) Phytases and phytase-labile organic phosphorus in manures and soils. Crit Rev Environ Sci Technol 43:916–954CrossRefGoogle Scholar
  27. Moore LR, Post AF, Rocap G, Chisholm SW (2002) Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47:989–996CrossRefGoogle Scholar
  28. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448CrossRefGoogle Scholar
  29. Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D (2000) Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182:291–296CrossRefGoogle Scholar
  30. Okada K, Kondo M, Ando H, Kakuda KI (2004) Phosphorus application affects root length distribution and water uptake of upland rice in a column experiment. Soil Sci Plant Nutr 50:257–261CrossRefGoogle Scholar
  31. Pansu M, Gautheyrou J (2007) Handbook of soil analysis: mineralogical, organic and inorganic methods. Springer Science & Business Media, HeidelbergGoogle Scholar
  32. Pikovskaya R (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370Google Scholar
  33. Postma J, Stevens LH, Wiegers GL, Davelaar E, Nijhuis EH (2009) Biological control of Pythium aphanidermatum in cucumber with a combined application of Lysobacter enzymogenes strain 3.1 T8 and chitosan. Biol Control 48:301–309CrossRefGoogle Scholar
  34. Reinhard C, Planavsky NJ, Gill BC, Ozaki K, Robbins LJ, Lyons TW, Fischer WW, Wang CJ, Cole DB, Konhauser KO (2017) Evolution of the global phosphorus cycle. Nature 541:386–389CrossRefGoogle Scholar
  35. Roos W, Luckner M (1984) Relationships between proton extrusion and fluxes of ammonium ions and organic acids in Penicillium cyclopium. Microbiology 130:1007–1014CrossRefGoogle Scholar
  36. Saneoka H (1989) Effects of phosphorus fertilizer on drought tolerance in warm season forage. J Jpn Grassl Sci 35:116–126Google Scholar
  37. Sharan A, Darmwal NS (2008) Efficient phosphorus solubilization by mutant strain of Xanthomonas campestris using different carbon, nitrogen and phosphorus sources. World J Microbiol Biotechnol 24:3087–3090CrossRefGoogle Scholar
  38. Srividya S, Soumya S, Pooja K (2009) Influence of environmental factors and salinity on phosphate solubilization by a newly isolated Aspergillus niger F7 from agricultural soil. Afr J Biotechnol 8:1864–1870Google Scholar
  39. Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270CrossRefGoogle Scholar
  40. Syers J, Johnston A, Curtin D (2008) Efficiency of soil and fertilizer phosphorus use: reconciling changing concepts of soil phosphorus behaviour with agronomic information vol 18. Food and agriculture Organization of the United Nations, Rome, ItalyGoogle Scholar
  41. Tabatabai M, Bremner J (1969) Use of ρ-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307CrossRefGoogle Scholar
  42. Tian LQ, Chen F, Sun BY (1991) Effects of high voltage electrostatic field on growth and metabolism of bacteria. Ind Water Treat 11:17–19Google Scholar
  43. Trolove S, Hedley M, Kirk G, Bolan N, Loganathan P (2003) Progress in selected areas of rhizosphere research on P acquisition. Soil Res 41:471–499CrossRefGoogle Scholar
  44. Vasilyeva NV, Tsfasman IM, Suzina NE, Stepnaya OA, Kulaev IS (2008) Secretion of bacteriolytic endopeptidase L5 of Lysobacter sp. XL1 into the medium by means of outer membrane vesicles. FEBS J 275:3827–3835CrossRefGoogle Scholar
  45. Volf CA, Ontkean GR, Bennett DR, Chanasyk DS, Miller JJ (2007) Phosphorus losses in simulated rainfall runoff from manured soils of Alberta. J Environ Qual 36:730–741CrossRefGoogle Scholar
  46. Wang Y, Qian G, Li Y, Wang Y, Wang Y, Wright S, Li Y, Shen Y, Liu F, Du L (2013) Biosynthetic mechanism for sunscreens of the biocontrol agent Lysobacter enzymogenes. PLoS One 8:e66633CrossRefGoogle Scholar
  47. Zaidi A, Khan MS, Ahemad M, Oves M, Wani P (2009) Recent advances in plant growth promotion by phosphatesolubilizing microbes. In: Khan MS (ed) Microbial strategies for crop improvement. Springer, Berlin, pp 23–50Google Scholar
  48. Zhou SX (2009) Effect of DC electrical stimulation on the growth process of bacteria. Dissertation, Capital Normal UniversityGoogle Scholar
  49. Zhu H, Wang YX, Hu BS, Liu FQ (2008) Cloning and expression of a chitinase gene from Lysobacter enzymogenes strain OH11. J Nanjing Agric Univ 31:47–50Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of Resources and EnvironmentSouthwest UniversityChongqingChina

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