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Streptomyces canus GLY-P2 degrades ferulic and p-hydroxybenzoic acids in soil and affects cucumber antioxidant enzyme activity and rhizosphere bacterial community

  • Fenghui Wu
  • Qinghua Shi
  • Xiu-Juan Wang
  • Zhong-Tao Sun
  • Wanying Wang
  • Xue Li
  • Li-Yuan Guo
  • Ji-Gang BaiEmail author
Regular Article
  • 155 Downloads

Abstract

Aims

The present study was conducted to investigate the effectiveness of Streptomyces (GLY-P2) in degradation of ferulic acid (FA) and p-hydroxybenzonic acid (PHBA) in the rhizosphere of cucumbers by assaying the alteration of antioxidant enzymes activities and rhizospheric microbial community.

Methods

GLY-P2 was isolated, identified as Streptomyces canus, and applied to cucumber-planted soil containing FA and PHBA.

Results

Optimal conditions for FA and PHBA degradation by GLY-P2 were 40 °C, pH 7, and 0.2 g l−1 mixture of FA and PHBA. During the degradation, vanillin, vanillic acid, and protocatechoic acid were metabolites; and activities of superoxide dismutase (SOD), catalase, ascorbate peroxidase (APX), and dehydroascorbate reductase in GLY-P2 were induced. When inoculated into cucumber-planted soil containing 220 μg g−1 mixture of FA and PHBA, GLY-P2 degraded FA and PHBA in soil, improved plant growth, and decreased malonaldehyde, superoxide radical, and hydrogen peroxide levels in leaves. GLY-P2 also enhanced activities of SOD, catalase, glutathione peroxidase, APX, monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase, increased contents of ascorbate and glutathione, and elevated transcript levels of copper/zinc SOD, manganese SOD, catalase, and APX in leaves. Moreover, GLY-P2 changed soil bacterial richness, diversity, and community composition, and increased phosphatase, catalase, urease, and sucrase activities in rhizospheric soil.

Conclusion

GLY-P2 mitigates FA and PHBA stress in cucumber by activating leaf antioxidant enzymes and affecting soil bacterial community.

Keywords

Antioxidant enzyme Bacterial community Cucumber Ferulic acid P-Hydroxybenzonic acid Streptomyces canus 

Supplementary material

11104_2018_3911_MOESM1_ESM.docx (7 mb)
ESM 1 (DOCX 7157 kb)

References

  1. Acostamartínez V, Dowd SE, Bell CW, Lascano R, Booker JD, Zobeck TM, Upchurch DR (2010) Microbial community composition as affected by dryland cropping systems and tillage in a semiarid sandy soil. Mol Divers 2:910–931CrossRefGoogle Scholar
  2. Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology. Academic press, Orlando, pp 121–126Google Scholar
  3. Amanatidou A, Smid EJ, Bennik MH, Gorris LG (2001) Antioxidative properties of Lactobacillus sake upon exposure to elevated oxygen concentrations. FEMS Microbiol Lett 203:87–94CrossRefGoogle Scholar
  4. Anupama VN, Amrutha PN, Chitra GS, Krishnakumar B (2008) Phosphatase activity in anaerobic bioreactors for wastewater treatment. Water Res 42:2796–2802CrossRefGoogle Scholar
  5. Balke NE (1985) Effects of allelochemicals on mineral uptake and associated physiological processes. ACS Symp Ser 268:161–178CrossRefGoogle Scholar
  6. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and assay applicable to acrylamide gels. Anal Biochem 44:276–278CrossRefGoogle Scholar
  7. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  9. Brunati M, Marinelli F, Bertolini C, Gandolfi R, Daffonchio D, Molinari F (2004) Biotransformations of cinnamic and ferulic acid with actinomycetes. Enzym Microb Technol 34:3–9CrossRefGoogle Scholar
  10. Chen L, Yang X, Raza W, Li J, Liu Y, Qiu M, Zhang F, Shen Q (2011) Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Appl Microbiol Biotechnol 89:1653–1663CrossRefGoogle Scholar
  11. Chen SY, Guo LY, Bai JG, Zhang Y, Zhang L, Wang Z, Chen JX, Yang HX, Wang XJ (2015) Biodegradation of p-hydroxybenzoic acid in soil by Pseudomonas putida CSY-P1 isolated from cucumber rhizosphere soil. Plant Soil 389:197–210CrossRefGoogle Scholar
  12. Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WR, Vance CV, Sarath G (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max L. Merr.) root nodules. Plant Physiol 102:481–489CrossRefGoogle Scholar
  13. De J, Sarkar A, Ramaiah N (2006) Bioremediation of toxic substances by mercury resistant marine bacteria. Ecotoxicology 15:385–389CrossRefGoogle Scholar
  14. Douglas LA, Bremner JM (1971) A rapid method of evaluating different compounds as inhibitors of urease activity in soils. Soil Biol Biochem 3:309–315CrossRefGoogle Scholar
  15. Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize leaves. Plant Physiol 114:1031–1037CrossRefGoogle Scholar
  16. Ferreira R, Gaspar H, Gonzalez JM, Clara MI, Santana MM (2015) Copper and temperature modify microbial communities, ammonium and sulfate release in soil. J Plant Nutr Soil Sc 178:953–962CrossRefGoogle Scholar
  17. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefGoogle Scholar
  18. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefGoogle Scholar
  19. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875CrossRefGoogle Scholar
  20. García C, Hernández T (1997) Biological and biochemical indicators in derelict soils subject to erosion. Soil Biol Biochem 29:171–177CrossRefGoogle Scholar
  21. Ghosh S, Sachan A, Sen SK, Mitra A (2007) Microbial transformation of ferulic acid to vanillic acid by Streptomyces sannanensis MTCC 6637. J Ind Microbiol Biotechnol 34:131–138CrossRefGoogle Scholar
  22. Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW (2013) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum, through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul 32:245–258CrossRefGoogle Scholar
  23. Huang YW, Zhou ZQ, Yang HX, Wei CX, Wan YY, Wang XJ, Bai JG (2015) Glucose application protects chloroplast ultrastructure in heat-stressed cucumber leaves through modifying antioxidant enzyme activity. Biol Plantarum 59:131–138CrossRefGoogle Scholar
  24. Jazayeri O, Aghajanzadeh TA, Gildeh BS (2007) Study of growth factors, alpha-amylase and peroxidase activity in various cultivars of rice (Oryza sativa L.) under vanillic acid stress. Pak J Biol Sci 10:1673–1678CrossRefGoogle Scholar
  25. Kohler J, Caravaca F, Roldan A (2009) Effect of drought on the stability of rhizosphere soil aggregates of Lactuca sativa grown in a degraded soil inoculated with PGPR and AM fungi. Appl Soil Ecol 42:160–165CrossRefGoogle Scholar
  26. Kumar V, Bharti A, Gusain O, Bisht GS (2011) Scanning electron microscopy of Streptomyces without use of any chemical fixatives. Scanning 33:446–469CrossRefGoogle Scholar
  27. Labeda D, Shearer M (1990) Isolation of actinomycetes for biotechnological applications. In: Labeda DP (ed) Isolation of biotechnological organisms from nature. McGraw-Hill Publishing Company, New York, pp 1–19Google Scholar
  28. Li DM, Nie YX, Zhang J, Yin JS, Li Q, Wang XJ, Bai JG (2013) Ferulic acid pretreatment enhances dehydration-stress tolerance of cucumber seedlings. Biol Plantarum 57:711–717CrossRefGoogle Scholar
  29. Liu ZJ, Guo YK, Bai JG (2010) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two cucumber ecotypes under osmotic stress. J Plant Growth Regul 29:171–183CrossRefGoogle Scholar
  30. Liu YJ, Liu SJ, Drake HL, Horn MA (2011) Alphaproteobacteria dominate active 2-methyl-4-chlorophenoxyacetic acid herbicide degraders in agricultural soil and drilosphere. Environ Microbiol 13:991–1009CrossRefGoogle Scholar
  31. Luster DG, Donaldson RP (1987) Orientation of electron transport activities in the membrane of intact glyoxysomes isolated from castor bean endosperm. Plant Physiol 85:796–800CrossRefGoogle Scholar
  32. Ma Y, Wang X, Wei M, Qi Y, Li T (2005) Accumulation of phenolic acids in continuously cropped cucumber soil and their effects on soil microbes and enzyme activities. Chinese J Appl Ecol 16:2149–2153Google Scholar
  33. Mattila P, Hellström J (2007) Phenolic acids in potatoes, vegetables, and some of their products. J Food Compost Anal 20:152–160CrossRefGoogle Scholar
  34. Max B, Carballo J, Cortés S, Domínguez JM (2012) Decarboxylation of ferulic acid to 4-vinyl guaiacol by Streptomyces setonii. Appl Biochem Biotechnol 166:289–299CrossRefGoogle Scholar
  35. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530CrossRefGoogle Scholar
  36. Muheim A, Lerch K (1999) Towards a high-yield bioconversion of ferulic acid to vanillin. Appl Microbiol Biotechnol 51:456–461CrossRefGoogle Scholar
  37. Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microbiol Ecol 53:110–122CrossRefGoogle Scholar
  38. Nojavan AM, Khorshidi M (2006) An investigation of vanillin imposed oxidative stress in corn (Zea mays L.) and the activities of antioxidative enzymes. Pak J Biol Sci 9:34–38CrossRefGoogle Scholar
  39. Pan C, Liu C, Zhao H, Wang Y (2013) Changes of soil physico-chemical properties and enzyme activities in relation to grassland salinization. Eur J Soil Biol 55:13–19CrossRefGoogle Scholar
  40. Ragot SA, Kertesz MA, Mészáros É, Frossard E, Bünemann EK (2017) Soil phoD and phoX alkaline phosphatase gene diversity responds to multiple environmental factors. FEMS Microbiol Ecol 93:118–120CrossRefGoogle Scholar
  41. Roberge MR (1978) Methodology of enzymes determination and extraction. In: Burns RG (ed) Soil enzymes. Academic Press, New York, pp 341–373Google Scholar
  42. Romero DM, de Molina MCR, Juárez ÁB (2011) Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotox Environ Safe 74:741–747CrossRefGoogle Scholar
  43. Salgado JM, Max B, Rodríguez-Solana R, Domínguez JM (2012) Purification of ferulic acid solubilized from agroindustrial wastes and further conversion into 4-vinyl guaiacol by Streptomyces setonii using solid state fermentation. Ind Crop Prod 39:52–61CrossRefGoogle Scholar
  44. Schinner F, Von Mersi W (1990) Xylanase, CM-cellulase and invertase activity in soil, an improved method. Soil Biol Biochem 22:511–515CrossRefGoogle Scholar
  45. Sun WJ, Nie YX, Gao Y, Dai AH, Bai JG (2012) Exogenous cinnamic acid regulates antioxidant enzyme activity and reduces lipid peroxidation in drought-stressed cucumber leaves. Acta Physiol Plant 34:641–655CrossRefGoogle Scholar
  46. Sutherland JB, Crawford DL, Pometto AL (1981) Catabolism of substituted benzoic acids by Streptomyces species. Appl Environ Microbiol 41:442–448Google Scholar
  47. Sutherland JB, Crawford DL, Pometto AL III (1983) Metabolism of cinnamic, p-coumaric and ferulic acids by Streptomyces setonii. Can J Microbiol 29:1253–1257CrossRefGoogle Scholar
  48. Tao K, Liu X, Chen X, Hu X, Cao L, Yuan X (2017) Biodegradation of crude oil by a defined co-culture of indigenous bacterial consortium and exogenous Bacillus subtilis. Bioresour Technol 224:327–332CrossRefGoogle Scholar
  49. Teng Y, Luo YM, Sun MM, Liu ZJ, Li ZG, Christie P (2010) Effect of bioaugmentation by Paracoccus sp. strain HPD-2 on the soil microbial community and removal of polycyclic aromatic hydrocarbons from an aged contaminated soil. Bioresour Technol 101:3437–3443CrossRefGoogle Scholar
  50. Turner JA, Rice EL (1975) Microbial decomposition of ferulic acid in soil. J Chem Ecol 1:41–58CrossRefGoogle Scholar
  51. Wan YY, Zhang Y, Zhang L, Zhou ZQ, Li X, Shi Q, Wang XJ, Bai JG (2015) Caffeic acid protects cucumber against chilling stress by regulating antioxidant enzyme activity and proline and soluble sugar contents. Acta Physiol Plant 37:1706CrossRefGoogle Scholar
  52. Wang FY, Lin XG, Yin R, Wu LH (2006) Effects of arbuscular mycorrhizal inoculation on the growth of Elsholtzia splendens and Zea mays and the activities of phosphatase and urease in a multi-metal-contaminated soil under unsterilized conditions. Appl Soil Ecol 31:110–119CrossRefGoogle Scholar
  53. Wang GL, Wang L, Chen HH, Shen B, Li SP, Jiang JD (2011) Lysobacter ruishenii sp. nov., a chlorothalonil-degrading bacterium isolated from a long-term chlorothalonil-contaminated soil. in China Int J Syst Evol Microbiol 61:674–679CrossRefGoogle Scholar
  54. Xu PL, Guo YK, Bai JG, Shang L, Wang XJ (2008a) Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. Physiol Plantarum 132:467–478CrossRefGoogle Scholar
  55. Xu S, Zhang S, You X, Jia X, Wu K (2008b) Degradation of soil phenolic acids by Phanerochaete chrysosporium under continuous cropping of cucumber. Chinese J Appl Ecol 19:2480–2484Google Scholar
  56. Xue T, Hartikainen H, Piironen V (2001) Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant Soil 237:55–61CrossRefGoogle Scholar
  57. Yu JQ (2001) Autotoxic potential of cucurbit crops: phenomenon, chemicals, mechanisms and means to overcome. J Crop Prod 4:335–348CrossRefGoogle Scholar
  58. Zhang Y, Wang XJ, Chen SY, Guo LY, Song ML, Feng H, Li C, Bai JG (2015) Bacillus methylotrophicus isolated from the cucumber rhizosphere degrades ferulic acid in soil and affects antioxidant and rhizosphere enzyme activities. Plant Soil 392:309–321CrossRefGoogle Scholar
  59. Zhang R, Lord DM, Bajaj R, Peti W, Page R, Sello JK (2017) A peculiar IclR family transcription factor regulates Para-hydroxybenzoate catabolism in Streptomyces coelicolor. Nucleic Acids Res 46:1501–1512CrossRefGoogle Scholar
  60. Zheng L, Zhang M, Xiao R, Chen J, Yu F (2016) Impact of salinity and Pb on enzyme activities of a saline soil from the Yellow River delta: a microcosm study. Phys Chem Earth 97:77–87CrossRefGoogle Scholar
  61. Zhou X, Yu G, Wu F (2012) Responses of soil microbial communities in the rhizosphere of cucumber (Cucumis sativus L.) to exogenously applied p-hydroxybenzoic acid. J Chem Ecol 38:975–983CrossRefGoogle Scholar
  62. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Fenghui Wu
    • 1
  • Qinghua Shi
    • 1
  • Xiu-Juan Wang
    • 2
  • Zhong-Tao Sun
    • 2
  • Wanying Wang
    • 2
  • Xue Li
    • 2
  • Li-Yuan Guo
    • 2
  • Ji-Gang Bai
    • 2
    Email author
  1. 1.State Key Laboratory of Crop Biology, College of Horticulture Science and EngineeringShandong Agricultural UniversityTai’anPeople’s Republic of China
  2. 2.State Key Laboratory of Crop Biology, College of Life SciencesShandong Agricultural UniversityTai’anPeople’s Republic of China

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