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Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation

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Abstract

To investigate the effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) on phytoremediation in saline-alkali soil contaminated by petroleum, saline-alkali soil samples were artificially mixed with different amount of oil, 5 and 10 g/kg, respectively. Pot experiments with oat plants (Avena sativa) were conducted under greenhouse condition for 60 days. Plant biomass, physiological parameters in leaves, soil enzymes, and degradation rate of total petroleum hydrocarbon were measured. The result demonstrated that petroleum inhibited the growth of the plant; however, inoculation with PGPR in combination with AMF resulted in an increase in dry weight and stem height compared with noninoculated controls. Petroleum stress increased the accumulation of malondialdehyde (MDA) and free proline and the activities of the antioxidant enzyme such as superoxide dismutase, catalase, and peroxidase. Application of PGPR and AMF augmented the activities of three enzymes compared to their respective uninoculated controls, but decreased the MDA and free proline contents, indicating that PGPR and AMF could make the plants more tolerant to harmful hydrocarbon contaminants. It also improved the soil quality by increasing the activities of soil enzyme such as urease, sucrase, and dehydrogenase. In addition, the degradation rate of total petroleum hydrocarbon during treatment with PGPR and AMF in moderately contaminated soil reached a maximum of 49.73 %. Therefore, we concluded the plants treated with a combination of PGPR and AMF had a high potential to contribute to remediation of saline-alkali soil contaminated with petroleum.

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Abbreviations

PGPR:

Plant growth promoting bacteria

AMF:

Arbuscular mycorrhizal fungi

MDA:

Malondialdehyde

TPH:

Total petroleum hydrocarbon

SOD:

Superoxide dismutase

CAT:

Catalase

POD:

Peroxidase

ROS:

Reactive oxygen species

References

  • Adesemoye A, Torbert H, Kloepper J (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58(4):921–929

    Article  CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 1631:73–181

    Google Scholar 

  • Alarcon A, Davies FT Jr, Autenrieth RL, Zuberer DA (2008) Arbuscular mycorrhiza and petroleum-degrading microorganisms enhance phytoremediation of petroleum-contaminated soil. Int J Phytoremediat 10(4):251–263

    Article  CAS  Google Scholar 

  • Allen R (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054

    CAS  Google Scholar 

  • Almaghrabi OA, Massoud SI, Abdelmoneim TS (2013) Influence of inoculation with plant growth promoting rhizobacteria (PGPR) on tomato plant growth and nematode reproduction under greenhouse conditions. Saudi J Biol Sci 20(1):57–61

    Article  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Asharf M, Foolad MR (2007) Role of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  Google Scholar 

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beauchamp CH, Fridovich I (1971) Superoxide dismutase: improved assays and assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Bowler C, Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116

    Article  CAS  Google Scholar 

  • Chang P, Gerhardt KE, Huang XD (2014) Plant growth-promoting bacteria facilitate the growth of barley and oats in salt-impacted soil: implications for phytoremediation of saline soils. Int J Phytoremediat 16(11):1133–1147

    Article  CAS  Google Scholar 

  • Chaudhry TM, Khan AG (2002) Role of symbiotic organisms in sustainable plant growth on heavy metal contaminated industrial sites. In: Rajak RC (ed) Biotechnology of microbes andsustainable utilization. Scientific Publishers, Jodhpur, pp 270–279

    Google Scholar 

  • Chaudhry TM, Khan AG (2003) In: Gorban GR, Lepp N (eds) Proceedings of the 7th international conference on the biogeochemistry of trace elements. Swedish University of Agricultural Sciences, Uppsala, pp 134–135

    Google Scholar 

  • Corgié SC, Beguiristain T, Leyval C (2006) Differential composition of bacterial communities as influenced by phenanthrene and dibenzo[a, h]anthracene in the rhizosphere of ryegrass (Lolium perenne L.). Biodegradation 17(6):511–521

    Article  Google Scholar 

  • Criquet S, Joner EJ, Léglize P, Leyval C (2000) Anthracene and mycorrhiza affect the activity of oxidoreductases in the roots and the rhizosphere of lucerne (Medicago sativa L.). Biotechnol Lett 22:1733–1737

    Article  CAS  Google Scholar 

  • Cunningham SD, Anderson TA, Schwab AP et al (1996) Phytoremediation of soils contaminated with organic pollutants. Adv Agron 56:55–114

    Article  CAS  Google Scholar 

  • del Rio LA, Sandalio LM, Altomare DA, Zilinskas BA (2003) Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. J Exp Bot 54:923–933

    Article  Google Scholar 

  • Dong R, Gu L, Guo C et al (2014) Effect of PGPR Serratia marcescens BC-3 and AMF Glomus intraradices on phytoremediation of petroleum contaminated soil. Ecotoxicology 23(4):674–680

    Article  CAS  Google Scholar 

  • Frankenberger WT, Johanson JB (1982) Influence of crude oil and refined petroleum products on soil dehydrogenase activity. J Environ Qual 11:602–607

    Article  CAS  Google Scholar 

  • García C, Hernández MT, Costa F (1997) Potential use of dehydrogenase activity as an index of microbial activity in degraded soils. Commun Soil Sci Plan 28:123–134

    Article  Google Scholar 

  • Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30

    Article  CAS  Google Scholar 

  • Glick BR, Stearns JC (2011) Making phytoremediation work better: maximizing a plant’s growth potential in the midst of adversity. Int J Phytoremediat 13(sup1):4–16

    Article  Google Scholar 

  • Gojgic-Cvijovic GD, Milic JS, Solevic TM et al (2012) Biodegradation of petroleum sludge and petroleum polluted soil by a bacterial consortium: a laboratory study. Biodegradation 23:1–14

    Article  CAS  Google Scholar 

  • Graj W, Lisiecki P, Szulc A et al (2013) Bioaugmentation with petroleum-degrading consortia has a selective growth-promoting impact on crop plants germinated in diesel oil-contaminated soil. Water Air Soil Poll 224(9):1–15

    Article  CAS  Google Scholar 

  • Guo J, Feng R, Ding Y et al (2014) Applying carbon dioxide, plant growth-promoting rhizobacterium and EDTA can enhance the phytoremediation efficiency of ryegrass in a soil polluted with zinc, arsenic, cadmium and lead. J Environ Manag 141:1–8

    Article  CAS  Google Scholar 

  • Gurska J, Wang W, Gerhardt KE et al (2009) Three year field test of a plant growth promoting rhizobacteria enhanced phytoremediation system at a land farm for treatment of hydrocarbon waste. Environ Sci Technol 43(12):4472–4479

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge J (1985) Free radicals in biology and medicine, 2nd edn. Oxford Clarendon Press, UK, pp 331–332

    Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434

    CAS  Google Scholar 

  • Herbinger K, Tausz M, Wonisch A, Soja G, Sorger A, Grill D (2002) Complex interactive effects of drought and ozone stress on the antioxidant defence systems of two wheat cultivars. Plant Physiol Biochem 40:691–696

    Article  CAS  Google Scholar 

  • Hong SH, Ryu HW, Kim J et al (2011) Rhizoremediation of diesel-contaminated soil using the plant growth promoting rhizobacterium Gordonia sp. S2RP-17. Biodegradation 22:593–601

    Article  CAS  Google Scholar 

  • Huang LL, Yang C, Zhao Y et al (2008) Antioxidant defenses of mycorrhizal fungus infection against SO2-induced oxidative stress in Avena nuda seedlings. B Environ Contam Tox 81(3):440–444

    Article  CAS  Google Scholar 

  • Huang XD, El-Alawi Y, Gurska J, Glick BR, Greenberg BM (2005) A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchem J 81:139–147

    Article  CAS  Google Scholar 

  • Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2004) A multi-process phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environ Pollut 130(3):465–476

    Article  CAS  Google Scholar 

  • Hutchinson SL, Banks MK, Schwab AP (2001) Phytoremediation of aged petroleum sludge: effect of inorganic fertilizer. J Environ Qual 30:395–403

    Article  CAS  Google Scholar 

  • Jaleel CA, Kishorekumar A, Manivannan P et al (2008) Salt stress mitigation by calcium chloride in Phyllanthus amarus. Acta Bot Croat 67:53–62

    CAS  Google Scholar 

  • Jamil M, Zeb S, Anees M et al (2014) Role of Bacillus licheniformis in phytoremediation of nickel contaminated soil cultivated with rice. Int J Phytoremediat 16(6):554–571

    Article  CAS  Google Scholar 

  • Janoušková M, Vosátka M (2005) Response to cadmium of Daucus carota hairy roots dual cultures with Glomus intraradices or Gigaspora margarita. Mycorrhiza 15:217–224

    Article  Google Scholar 

  • Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33(3):797–802

    Article  Google Scholar 

  • Joner EJ, Leyval C (2003) Rhizosphere gradients of polycyclicaromatic hydrocarbon (PAH) dissipation in two industrial soils, and the impact of arbuscular mycorrhiza. Environ Sci Technol 37:2371–2375

    Article  CAS  Google Scholar 

  • Keshavkant S, Padhan J, Parkhey S et al (2012) Physiological and antioxidant responses of germinating Cicer arietinum seeds to salt stress. Russ J Plant Physiol 59:206–211

  • Kohler J, Caravaca F, Carrasco L, Roldan A (2007) Interactions between a plant growth-promoting rhizobacterium, an AM fungus and a phosphate-solubilising fungus in the rhizosphere of Lactuca sativa. Appl Soil Ecol 35:480–487

    Article  Google Scholar 

  • Kohler J, Hernández JA, Caravaca F et al (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252

    Article  CAS  Google Scholar 

  • Kumari B, Singh SN (2011) Phytoremediation of metals from fly ash through bacterial augmentation. Ecotoxicology 20(1):166–176

    Article  CAS  Google Scholar 

  • Langella F, Grawunder A, Stark R (2013) Microbially assisted phytoremediation approaches for two multi-element contaminated sites. Environ Sci Pollut R:1–14

  • Langella F, Grawunder A, Stark R et al (2014) Microbially assisted phytoremediation approaches for two multi-element contaminated sites. Environ Sci Pollut R 21(11):6845–6858

    Article  CAS  Google Scholar 

  • Li QL, Ling WT, Gao YZ (2006) Arbuscular mycorrhizal bioremediation and its mechanisms of organic pollutants-contaminated soils. Chin J Appl Ecol 17:2217–2221

    CAS  Google Scholar 

  • Lin X, Li X, Li P, Li F, Zhang L, Zhou Q (2008) Evaluation of plant–microorganism synergy for the remediation of diesel fuel contaminated soil. B Environ Contam Tox 81(1):19–24

    Article  CAS  Google Scholar 

  • Liu W, Sun J, Ding L et al (2013) Rhizobacteria (Pseudomonas sp. SB) assist phytoremediation of oily-sludge-contaminated soil by tall fescue (Testuca arundinacea L.). Plant Soil 371:533–542

    Article  CAS  Google Scholar 

  • Mäder P, Kaiser F, Adholeya A et al (2011) Inoculation of root microorganisms for sustainable wheat–rice and wheat–black gram rotations in India. Soil Biol Biochem 43(3):609–619

  • Marques APGC, Moreira H, Franco AR et al (2013) Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria—effects on phytoremediation strategies. Chemosphere 92(1):74–83

    Article  CAS  Google Scholar 

  • Moerschbacher BM, Noll UM, Flott BE (1998) Lignin biosynthetic enzymes in stem rust infected, resistance and susceptible near-isogenic wheat lines. Ann Mol Pathol 33(1):33–46

    Google Scholar 

  • Muratova AY, Dmitrieva TV, Panchenko LV, Turkovskaya OV (2008) Phytoremediation of oil-sludge-contaminated soil. Int J Phytoremediat 10:486–502

    Article  CAS  Google Scholar 

  • Nannipieri P, Ceccanti B, Cervelli S et al (1980) Extraction of phosphatase, urease, protease, organic carbon and nitrogen from soil. Soil Sci Soc Am J 44:1011–1016

    Article  CAS  Google Scholar 

  • Ordookhani K, Khavazi K, Moezzi A, Rejali F (2010) Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr J Agric Res 5(10):1108–1116

    Google Scholar 

  • Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 49:157–165

    Article  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  CAS  Google Scholar 

  • Reed ML, Glick BR (2005) Growth of canola (Brassica napus) in the presence of plant growth-promoting bacteria and either copper or polycyclic aromatic hydrocarbons. Can J Microbiol 51(12):1061–1069

    Article  CAS  Google Scholar 

  • Robert FM, Sun WH, Toma M, Jones RK, Tang CS (2008) Interactions among buffelgrass, phenanthrene and phenanthrene-degrading bacteria in gnotobiotic microcosms. J Environ Sci Heal A 43(9):1035–1041

    Article  CAS  Google Scholar 

  • Saba H, Jyoti P, Neha S (2013) Mycorrhizae and phytochelators as remedy in heavy metal contaminated land remediation. Int Res J Environ Sci 2(1):74–78

    Google Scholar 

  • Sugiura K, Ishihara M, Harayama ST (1997) Physicochemical properties and biodegradability of crude oil. Environ Sci Technol 31:45–51

    Article  CAS  Google Scholar 

  • Tang J, Wang R, Niu X, Wang M, Zhou Q (2010) Characterization on the rhizoremediation of petroleum contaminated soil as affected by different influencing factors. Biogeosci Discuss 7(3)

  • Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228

    Article  CAS  Google Scholar 

  • Unterbrunner R, Wieshammer G, Hollender U, Felderer B, Wieshammer-Zivkovic M, Puschenreiter M, Wenzel WW (2007) Plant and fertiliser effects on rhizodegradation of crude oil in two soils with different nutrient status. Plant Soil 300:117–126

    Article  CAS  Google Scholar 

  • Wang Y, Tang M, Guo Y et al (2006) Inoculation effect of ectomycorrhizal fungi on Cunninghamia lanceolata. Acta Bot Boreali-Occidentalia Sin 26:1900–1904

    CAS  Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant assisted bioremediation (phytoremediation) of soils. Plant Soil 321(1–2):385–408

    Article  CAS  Google Scholar 

  • Yateem A (2013) Rhizoremediation of oil-contaminated sites: a perspective on the Gulf War environmental catastrophe on the State of Kuwait. Environ Sci Pollut R 20(1):100–107

    Article  CAS  Google Scholar 

  • Zhou QX, Cai Z, Zhang ZN et al (2011) Ecological remediation of hydrocarbon contaminated soils with weed plant. J Resour Ecol 2(2):97–105

    Google Scholar 

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Acknowledgments

This study was supported by the National Natural Science Foundation of China (31170479), Programs for Science and Technology Development of Heilongjiang Province, China (Grant No. GC12B304), Aid Program for Science and Technology Innovative Research Team in Higher Educational Institutions of Heilongjiang Province (2010TD10), and Harbin Normal University (KJTD2011-2).

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Authors and Affiliations

  1. Key Laboratory of Molecular and Cytogenetics, Heilongjiang Province, College of Life Science and Technology, Harbin Normal University, Harbin, 150025, China

    Feifei Xun, Baoming Xie, Shasha Liu & Changhong Guo

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  1. Feifei Xun
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  2. Baoming Xie
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  3. Shasha Liu
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  4. Changhong Guo
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Correspondence to Changhong Guo.

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Responsible editor: Robert Duran

Feifei Xun and Baoming Xie contributed equally to this paper.

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Xun, F., Xie, B., Liu, S. et al. Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22, 598–608 (2015). https://doi.org/10.1007/s11356-014-3396-4

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