Skip to main content
Log in

Phytoremediation using microbially mediated metal accumulation in Sorghum bicolor

  • Alteration and element mobility at the microbe-mineral interface
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Reclaiming land that has been anthropogenically contaminated with multiple heavy metal elements, e.g., during mining operations, is a growing challenge worldwide. The use of phytoremediation has been discussed with varying success. Here, we show that a careful examination of options of microbial determination of plant performance is a key element in providing a multielement remediation option for such landscapes. We used both (a) mycorrhiza with Rhizophagus irregularis and (b) bacterial amendments with Streptomyces acidiscabies E13 and Streptomyces tendae F4 to mediate plant-promoting and metal-accumulating properties to Sorghum bicolor. In pot experiments, the effects on plant growth and metal uptake were scored, and in a field trial at a former uranium leaching heap site near Ronneburg, Germany, we could show the efficacy under field conditions. Different metals could be extracted at the same time, with varying microbial inoculation and soil amendment scenarios possible when a certain metal is the focus of interest. Especially, manganese was extracted at very high levels which might be useful even for phytomining approaches.

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

Similar content being viewed by others

References

  • Abbas A, Edwards C (1989) Effects of metals on a range of Streptomyces species. Appl Env Microbiol 55:2030–2035

    CAS  Google Scholar 

  • Abdel-Fattah GM, Mohamedin AH (2000) Interactions between a vesicular-arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32:401–409

    Article  Google Scholar 

  • Abou-Shanab RA, Ghanem K, Ghanem N, Al-Kolaibe A (2008) The role of bacteria on heavy-metal extraction and uptake by plants growing on multi-metal-contaminated soils. World J Microbiol Biotechnol 24:253–262

    Article  CAS  Google Scholar 

  • Adriano-Anaya ML, Salvador-Figueroa M, Ocampo JA, Garcia-Romera I (2006) Hydrolytic enzyme activities in maize (Zea mays) and sorghum (Sorghum bicolor) roots inoculated with Gluconacetobacter diazotrophicus and Glomus intraradices. Soil Biol Biochem 38:879–886

    Article  CAS  Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20

    Article  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881

    Article  CAS  Google Scholar 

  • Ames RN, Reid CPP, Ingham ER (1984) Rhizosphere bacterial population responses to root colonization by a vesicular arbuscular mycorrhizal fungus. New Phytol 96:555–563

    Article  Google Scholar 

  • Amoroso MJ, Schubert D, Mitscherlich P, Schumann P, Kothe E (2000) Evidence for high affinity nickel transporter genes in heavy metal resistant Streptomyces spec. J Basic Microbiol 40:295–301

    Article  CAS  Google Scholar 

  • Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation—an overview. Crit Rev Plant Sci 24:109–122

    Article  CAS  Google Scholar 

  • Baker AJM, McGrath SP, Sidoli CMD, Reeves RD (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Res Conserv Recycl 11:41–49

    Article  Google Scholar 

  • Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal(loid)s contaminated soils—to mobilize or to immobilize? J Hazard Mat 266:141–166

    Article  CAS  Google Scholar 

  • Brunetti G, Farrag K, Rovira PS, Nigro F, Senesi N (2011) Greenhouse and field studies on Cr, Cu, Pb and Zn phytoextraction by Brassica napus from contaminated soils in the Apulia region, Southern Italy. Geoderma 160:517–523

    Article  CAS  Google Scholar 

  • Büchel G, Bergmann H, Ebenå G, Kothe E (2005) Geomicrobiology in remediation of mine waste. Chem Erde – Geochem 65:1–5

    Article  Google Scholar 

  • Ciura J, Poniedzialek M, Sekara A, Jedrszczyk E (2005) The possibility of using crops as metal phytoremediants. Pol J Env Stud 14:17–22

    CAS  Google Scholar 

  • Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25

    Article  CAS  Google Scholar 

  • Dimkpa CO, Merten D, Svatos A, Buchel G, Kothe E (2009a) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696

    Article  CAS  Google Scholar 

  • Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E (2009b) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162

    Article  CAS  Google Scholar 

  • Dushenkov S, Kapulnik Y, Blaylock M, Sorochisky B, Raskin I, Ensley B (1997) Phytoremediation: a novel approach to an old problem. In: Wise DL (ed) Studies in environmental science. Elsevier, Amsterdam, pp 563–572

    Google Scholar 

  • Epelde L, Mijangos I, Becerril JM, Garbisu C (2009) Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol Biochem 41:1788–1794

    Article  CAS  Google Scholar 

  • Ernst WHO (2005) Phytoextraction of mine wastes—options and impossibilities. Chem Erde – Geochem 65:29–42

    Article  CAS  Google Scholar 

  • Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534

    CAS  Google Scholar 

  • Grawunder A, Lonschinski M, Merten D, Büchel G (2009) Distribution and bonding of residual contamination in glacial sediments at the former uranium mining leaching heap of Gessen/Thuringia, Germany. Chem Erde – Geochem 69S2:5–19

    Article  Google Scholar 

  • Griffioen WAJ (1994) Characterization of a heavy metal-tolerant endomycorrhizal fungus from the surroundings of a zinc refinery. Mycorrhiza 4:197–200

    Article  CAS  Google Scholar 

  • Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467

    Article  CAS  Google Scholar 

  • Hernández-Allica J, Becerril JM, Garbisu C (2008) Assessment of the phytoextraction potential of high biomass crop plants. Env Poll 152:32–40

    Article  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  CAS  Google Scholar 

  • Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207

    Article  CAS  Google Scholar 

  • Langella F, Grawunder A, Stark R, Weist A, Merten D, Haferburg G, Büchel G, Kothe E (2014) Microbially assisted phytoremediation approaches for two multi-element contaminated sites. Env Sci Poll Res 21:6845–6858

    Article  CAS  Google Scholar 

  • Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Env Qual 31:109–120

    Article  CAS  Google Scholar 

  • Marchiol L, Fellet G, Perosa D, Zerbi G (2007) Removal of trace metals by Sorghum bicolor and Helianthus annuus in a site polluted by industrial wastes: a field experience. Plant Physiol Biochem 45:379–387

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214

    Article  CAS  Google Scholar 

  • Murillo JM, Maranon T, Cabrera F, Lopez R (1999) Accumulation of heavy metals in sunflower and sorghum plants affected by the Guadiamar spill. Sci Total Env 242:281–292

    Article  CAS  Google Scholar 

  • Neagoe A, Ebena G, Carlsson E (2005) The effect of soil amendments on plant performance in an area affected by acid mine drainage. Chem Erde – Geochem 65:115–129

    Article  CAS  Google Scholar 

  • Neagoe A, Stancu P, Onete M, Bodescu F, Gheorghe R, Iordache V (2014) Effects of arbuscular mycorrhizal fungi on Agrostis capillaris grown on amended mine tailing substrate at pot, lysimeter, and field plot scales. Environ Sci Pollut Res 21:6859–6876

    Article  CAS  Google Scholar 

  • Nogueira MA, Nehls U, Hampp R, Poralla K, Cardoso E (2007) Mycorrhiza and soil bacteria influence extractable iron and manganese in soil and uptake by soybean. Plant Soil 298:273–284

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221–226

    Article  CAS  Google Scholar 

  • Rojas-Tapias D, Bonilla R, Dussán J (2012) Effect of inoculation with plant growth-promoting bacteria on growth and copper uptake by sunflowers. Water Air Soil Pollut 223:643–654

    Article  CAS  Google Scholar 

  • Saraswat S, Rai JPN (2009) Phytoextraction potential of six plant species grown in multimetal contaminated soil. Chem Ecol 25:1–11

    Article  CAS  Google Scholar 

  • Schindler F, Gube M, Kothe E (2012) Bioremediation and heavy metal uptake: microbial applications at field scale. In: Kothe E, Varma A (eds) Bio-geo interactions in metal contaminated soils. Springer, Heidelberg, pp 365–384

    Chapter  Google Scholar 

  • Schmidt A, Haferburg G, Sineriz M, Merten D, Büchel G, Kothe E (2005) Heavy metal resistance mechanisms in actinobacteria for survival in AMD contaminated soils. Chem Erde – Geochem 65:131–144

    Article  CAS  Google Scholar 

  • Schmidt A, Haferburg G, Schmidt A, Lischke U, Merten D, Ghergel F, Büchel G, Kothe E (2009) Heavy metal resistance to the extreme: Streptomyces strains from a former uranium mining area. Chem Erde – Geochem 69:35–44

    Article  CAS  Google Scholar 

  • Schreiner RP, Koide RT (1993) Streptomycin reduces plant response to mycorrhizal infection. Soil Biol Biochem 25:1131–1133

    Article  CAS  Google Scholar 

  • Schütze E, Klose M, Merten D, Nietzsche S, Senftleben D, Roth M, Kothe E (2014) Growth of streptomycetes in soil and their impact on bioremediation. J Hazard Mater 267:128–135

    Article  Google Scholar 

  • Sessitsch A, Kuffner M, Kidd P, 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  Google Scholar 

  • Sheng X, Sun L, Huang Z, He L, Zhang W, Chen Z (2012) Promotion of growth and Cu accumulation of bio-energy crop (Zea mays) by bacteria: implications for energy plant biomass production and phytoremediation. J Env Manag 103:58–64

    Article  CAS  Google Scholar 

  • Sullivan TS, McBride MB, Thies JE (2013) Rhizosphere microbial community and Zn uptake by willow (Salix purpurea L.) depend on soil sulfur concentrations in metalliferous peat soils. Appl Soil Ecol 67:53–60

    Article  Google Scholar 

  • Toler HD, Morton JB, Cumming JR (2005) Growth and metal accumulation of mycorrhizal sorghum exposed to elevated copper and zinc. Water Air Soil Poll 164:155–172

    Article  CAS  Google Scholar 

  • Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174

    Article  CAS  Google Scholar 

  • Usman ARA, Mohamed HM (2009) Effect of microbial inoculation and EDTA on the uptake and translocation of heavy metal by corn and sunflower. Chemosphere 76:893–899

    Article  CAS  Google Scholar 

  • Vamerali T, Bandiera M, Mosca G (2009) Field crops for phytoremediation of metal-contaminated land. Env Chem Lett 8:1–17

    Article  Google Scholar 

  • Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr 10:268–292

    Article  Google Scholar 

  • Wang FY, Lin XG, Yin R (2007) Inoculation with arbuscular mycorrhizal fungus Acaulospora mellea decreases Cu phytoextraction by maize from Cu-contaminated soil. Pedobiologia 51:99–109

    Article  CAS  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598

    Article  CAS  Google Scholar 

  • Yang X, Feng Y, He Z, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353

    Article  CAS  Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Env 368:456–464

    Article  CAS  Google Scholar 

  • Zeien H, Brümmer G (1989) Chemische Extraktionen zur Bestimmung von Schwermetallbindungsformen in Böden. Mitt Dtsch Bodenkundl Ges 59:505–510

    Google Scholar 

  • Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43

    Article  CAS  Google Scholar 

  • Zhuang P, Yang QW, Wang HB, Shu WS (2007a) Phytoextraction of heavy metals by eight plant species in the field. Water Air Soil Poll 184:235–242

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Zhuang P, Shu W, Li Z, Liao B, Li J, Shao J (2009) Removal of metals by sorghum plants from contaminated land. J Env Sci 21:1432–1437

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the Research Training Group (DFG-Gk1257) and the Excellence Graduate School for Microbial Communication (JSMC) for financial support. We are grateful to Dr. Hubert Schröter (TLL, Jena), Ulrike Buhler and Ines Kamp (Applied Geology, FSU Jena), Benjamin Funai (Microbial Communication, FSU Jena), and Dr. Christine Fischer (Ecohydrology, FSU Jena) for assistance and help with this interdisciplinary work.

Conflict of interest

There are no potential conflicts of interest.

Compliance with ethical standards

This research does not involve human participants or animals.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erika Kothe.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Phieler, R., Merten, D., Roth, M. et al. Phytoremediation using microbially mediated metal accumulation in Sorghum bicolor . Environ Sci Pollut Res 22, 19408–19416 (2015). https://doi.org/10.1007/s11356-015-4471-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4471-1

Keywords

Navigation