Skip to main content
Log in

Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aim

Phytomining is the conception of agro-metallurgical production chains based on cropping hyperaccumulator plants on contaminated or naturally rich (ultramafic) soils to produce high value metal compounds. This study aimed to evaluate the effect of enhancing multispecies hyperaccumulator covers with Plant Growth Promoting Rhizobacteria (PGPR) on Ni phytoextraction.

Method

Plant growth promoting rhizobacteria were isolated from the rhizosphere of two different plant associations (Bornmuellera tymphaea - Noccaea tymphaea (NB) and Bornmuellera tymphaea - Alyssum murale (AB)) collected from natural conditions. The screening of isolates from both plant associations for their PGPR traits revealed two PGPR strains (AB30 and NB24) affiliated to Variovorax paradoxus. Inoculation of mesocosms containing the same plant associations with these selected PGPR was performed after 5 months of culture. The biomass of the different plant parts and respective concentrations of nickel in the plants were recorded 1 month after inoculation.

Results

Root biomass of the inoculated plant associations was significantly higher than the respective non-inoculated ones. The total biomass of the inoculated plant association Bornmuellera tymphaea - Noccaea tymphaea was significantly higher than the total biomass of all others. Similarly, shoot biomass of the inoculated plant association B. tymphaea - N. tymphaea was significantly higher than that of all other covers. Results showed an increase in Ni uptake when plants were inoculated with PGPR strains, when compared with uninoculated plant associations. According to the plant cover, the inoculation increased Ni amounts in roots of 105.8 and 66.4 % respectively in ABi and NBi covers, and 39.9 and 79.6 % in the shoots.

Conclusion

The combination of the hyperaccumulator plants N. tymphaea-B.tymphaea inoculated by one of the two PGPR strains (strain NB24), isolated from the rhizosphere of this mixed cover, seemed to be an interesting option for an efficient Ni phytoextraction to be tested in the field.

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

Similar content being viewed by others

References

  • Aboudrar W, Schwartz C, Benizri E, Morel JL, Boularbah A (2007) Soil microbial diversity as affected by the rhizosphere of the hyperaccumulator Thlaspi caerulescens under natural conditions. Int J Phytorem 9:41–52

    Article  CAS  Google Scholar 

  • Aboudrar W, Schwartz C, Morel JL, Boularbah A (2012) Effect of nickel-resistant rhizosphere bacteria on the uptake of nickel by the hyperaccumulator Noccaea caerulescens under controlled conditions. J Soil Sediments 13:501–507

    Article  Google Scholar 

  • Abou-Shanab R, Angle J, Delorme T, Chaney R, van Berkum P, Moawa H, Ghanem K, Ghozlan H (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224

    Article  CAS  Google Scholar 

  • Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889

    Article  CAS  Google Scholar 

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45

    Article  CAS  Google Scholar 

  • Bani A, Echevarria G, Mullaj A, Reeves R, Morel JL, Sulçe S (2009) Nickel hyperaccumulation by brassicaceae in serpentine soils of Albania and Northwestern Greece. Soil and biota of serpentine: a world view. Northeast Nat 16:385–404

    Article  Google Scholar 

  • Bani A, Echevarria G, Sulçe S, Morel JL (2015) Improving the agronomy of Alyssum murale for extensive phytomining : a five-year field study. Int J Phytorem 17:117–127

    Article  CAS  Google Scholar 

  • Barillot C (2012) Etude des potentialités rhizoremédiatrices et de la diversité des bactéries rhizosphériques d’Arabidopsis halleri, plante hyperaccumulatrice de Zn et Cd. Thèse de l’Université de Technologie de Compiègne, 237 pp

  • Becerra-Castro C, Monterroso C, Prieto-Fernández A, Rodríguez-Lamas L, Loureiro-Viñas M, Acea MJ, Kidd PS (2012) Pseudometallophytes colonising Pb/Zn mine tailings: a description of the plant-microorganism-rhizosphere soil system and isolation of metal-tolerant bacteria. J Haz Mat 217–218:350–359

    Article  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Benizri E, Amiaud B (2005) Relationship between plants and soil microbial communities in fertilized grasslands. Soil Biol Biochem 37:2055–2064

    Article  CAS  Google Scholar 

  • Blossfeld S, Perriguey J, Sterckeman T, Morel JL, Lösch R (2009) Rhizosphere pH dynamics in trace-metal-contaminated soils, monitored with planar pH optodes. Plant Soil 330:173–184

    Article  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    Article  CAS  PubMed  Google Scholar 

  • Cabello-Conejo MI, Becerra-Castro C, Prieto-Fernández A, Monterroso C, Saavedra-Ferro A, Mench M, Kidd PS (2014) Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant Soil 1–2:35–50

    Article  Google Scholar 

  • Chaney RL, Chen KY, Li YM, Angle JS, Baker AJM (2008) Effects of calcium on nickel tolerance and accumulation in Alyssum species and cabbage grown in nutrient solution. Plant Soil 311:131–140

    Article  CAS  Google Scholar 

  • Dell’Amico E, Cavalca EL, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84

    Article  Google Scholar 

  • Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng THB, Tang YT, Morel JL (2015) Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett 423:24–25

    Article  CAS  Google Scholar 

  • Gao Y, Miao C, Xia J, Mao L, Wang Y, Zhou P (2012) Plant diversity reduces the effect of multiple heavy metal pollution on soil enzyme activities and microbial community structure. Front Environ Sci Eng 6:213–223

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  PubMed  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    Article  CAS  PubMed  Google Scholar 

  • Gove B, Hutchinson JJ, Young SD, Craigon J, McGrath SP (2002) Uptake of metals by plants sharing a rhizosphere with the hyperaccumulator Thlaspi caerulescens. Int J Phytorem 4:267–281

    Article  CAS  Google Scholar 

  • Gürtler V, Stanisich VA (1996) New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 142:3–16

    Article  PubMed  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  • Ibekwe AM, Kennedy AC (1999) Fatty acid methyl ester (FAME) profiles as a tool to investigate community structure of two agricultural soils. Plant Soil 206:151–161

    Article  Google Scholar 

  • Jacobson CB, Pasternak JJ, Glick BR (1994) Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 40:1019–1025

    Article  CAS  Google Scholar 

  • Jiang C, Wu QT, Sterckeman T, Schwartz C, Sirguey C, Ouvrard S, Perriguey J, Morel JL (2010) Co-planting can phytoextract similar amounts of cadmium and zinc to mono-cropping from contaminated soils. Ecol Eng 36:391–395

    Article  Google Scholar 

  • Jiang F, Chen L, Belimov AA, Shaposhnikov A, Gong F, Meng X, Hartung W, Jeschke D, Davies W, Dodd I (2012) Multiple impacts of the plant growth-promting rhizobacterium Variovorax paradoxus 5C-2 on nutrient and ADB relations of Pisum sativum. J Exp Bot 63:695–709

    Article  Google Scholar 

  • Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522

    Article  CAS  PubMed  Google Scholar 

  • Lindsay WL, Norvell WA (1978) Development of DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • Liu YG, Ye F, Zeng GM, Fan T, Meng L, Yuan HS (2007) Effects of added Cd on Cd uptake by oilseed rape and pai-tsai co-cropping. Trans Nonferrous Metals Soc China 17:846–852

    Article  CAS  Google Scholar 

  • Lucisine P, Echevarria G, Sterckeman T, Vallance J, Rey P, Benizri E (2014) Effect of hyperaccumulating plant cover composition and rhizosphere-associated bacteria on the efficiency of nickel extraction from soil. Appl Soil Ecol 81:30–36

    Article  Google Scholar 

  • Ma JF, Nomoto K (1993) Inhibition of mugineic acid-ferric complex uptake in barley by copper, zinc and cobalt. Physiol Plant 89:331–334

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75:719–725

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Luo YM, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants effects on plant growth and Ni uptake. J Hazard Mater 195:230–237

    Article  CAS  PubMed  Google Scholar 

  • Magurran AE (2003) Measuring biological diversity. 2003, Wiley-Blackwell Publishing, 264pp

  • Miwa H, Ahmed I, Yoon J, Yokota A, Fujiwara T (2008) Variovorax boronicumulans sp. nov., a boron-accumulating bacterium isolated from soil. Int J Syst Evol Microbiol 58:286–289

    Article  CAS  PubMed  Google Scholar 

  • Orhan E, Esitken A, Ercisli S, Turan M, Sahin F (2006) Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Sci Hortic 111:38–43

    Article  CAS  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574

    Article  CAS  PubMed  Google Scholar 

  • Rue M, Vallance J, Echevarria G, Rey P, Benizri E (2015) Rhizosphere microbial communities under mono- or multispecies hyperaccumulator plant cover in a serpentine soil. Aust J Bot 63:92–102

    CAS  Google Scholar 

  • Sarwar M, Arshad M, Martens DA, Frankenberger WT Jr (1992) Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147:207–215

    Article  CAS  Google Scholar 

  • Schlegel HG, Cosson JP, Baker AJM (1991) Nichel-hyperaccumulating plants provide a niche for nickel-resistant bacteria. Bot Acta 104:18–25

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Sessitsch A, Kuffner M, Kidd PS, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaharoona B, Arshad M, Zahir M, Khalid A (2006) Performance of Pseudomonas spp. containing ACC-deaminase for improving growth and yield of maize (Zea mays L.) in the presence of nitrogenous fertilizer. Soil Biol Biochem 38:2971–2975

    Article  CAS  Google Scholar 

  • Shahzad SM, Khalid A, Arshad M, Tahir J, Mahmood T (2010) Improving nodulation, growth and yield of Cicer arietinum L. through bacterial ACC-deaminase induced changes in root architecture. Eur J Soil Biol 46:342–347

    Article  CAS  Google Scholar 

  • Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale (Waldst. & Kit.). S Afr J Sci 97:568–570

    CAS  Google Scholar 

  • Smaill SJ, Leckie AC, Clinton PW, Hickson AC (2010) Plantation management induces long-term alterations to bacterial phytohormone production and activity in bulk soil. Appl Soil Ecol 45(3):310–314

    Article  Google Scholar 

  • Tappero R, Peltier E, Grӓfe M, Heidel K, Ginder-Vogel M, Livi KJT, Rivers ML, Marcus MA, Chaney RL, Sparks DL (2007) Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol 175:641–654

    Article  CAS  PubMed  Google Scholar 

  • Teixeira DA, Alfenas AC, Mafia RG, Ferreira EM, De Siqueira L, Maffia LA, Mounteer AH (2007) Rhizobacterial promotion of eucalypt rooting and growth. Braz J Microbiol 38:118–123

    Article  Google Scholar 

  • Turgay OC, Görmez A, Bilen S (2012) Isolation and characterization of metal resistant-tolerant rhizosphere bacteria from the serpentine soils in Turkey. Environ Monit Assess 184:515–526

    Article  CAS  PubMed  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccu-mulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Article  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson C, Meech J, Erskine P, Simonnot MO, Vaughan J, Morel JL, Echevarria G, Fogliani B, Mulligan D (2015) Agromining: farming for metals in the future? Environ Sci Technol. doi:10.1021/es50601u

    PubMed  Google Scholar 

  • Visioli G, d’Egidio S, Vamerali T, Mattarozzi M, Sanangelantoni AM (2014) Culturable endophytic bacteria enhance Ni translocation in the hyperaccumulator Noccaea caerulescens. Chemosphere 117:538–544

    Article  CAS  PubMed  Google Scholar 

  • Wei ZB, Guo XF, Wu QT, Long XX, Penn CJ (2011) Phytoextraction of heavy metals from contaminated soil by co-cropping with chelator application and assessment of associated leaching risk. Int J Phytorem 13:717–729

    Article  CAS  Google Scholar 

  • Wöhler I (1997) Auxin-indole derivatives in soils determined by a colorimetric method and by high performance liquid chromatography. Microbiol Res 152:399–405

    Article  Google Scholar 

  • Wu QT, Hei L, Wong JWC, Schwartz C, Morel JL (2007) Co-cropping for phyto-separation of zinc and potassium from sewage sludge. Chemosphere 68:1954–1960

    Article  CAS  PubMed  Google Scholar 

  • Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation of trace elements by wetland plants. I. Duck weed. J Environ Qual 27:715–721

    Article  CAS  Google Scholar 

  • Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Benizri.

Additional information

Responsible Editor: Fangjie Zhao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Durand, A., Piutti, S., Rue, M. et al. Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria. Plant Soil 399, 179–192 (2016). https://doi.org/10.1007/s11104-015-2691-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2691-2

Keywords

Navigation