Environmental Science and Pollution Research

, Volume 23, Issue 21, pp 21327–21335 | Cite as

Aseptic hydroponics to assess rhamnolipid-Cd and rhamnolipid-Zn bioavailability for sunflower (Helianthus annuus): a phytoextraction mechanism study

  • Jia Wen
  • Mike J. McLaughlin
  • Samuel P. Stacey
  • Jason K. Kirby
Research Article

Abstract

The availability of cadmium (Cd) and zinc (Zn) to sunflower (Helianthus annuus) was investigated in rhamnolipid- and ethylenediaminetetraacetic acid (EDTA)-buffered solutions in order to evaluate the influence of aqueous speciation of the metals on their uptake by the plant, in relation to predictions of uptake by the free ion activity model (FIAM). Free metal ion activity was estimated using the chemical equilibrium program MINTEQ or measured by Donnan dialysis. The uptake of Cd followed the FIAM for the EDTA-buffered solution at EDTA concentrations below 0.4 μM; for the rhamnolipid-buffered solution, the uptake of both metals in roots was not markedly affected by increasing rhamnolipid concentrations in solution. This suggests rhamnolipid enhanced metal accumulation in plant roots (per unit free metal in solution) possibly through formation and uptake of lipophilic complexes. The addition of normal Ca concentrations (low millimetre range) to the rhamnolipid uptake solutions reduced Cd accumulation in shoots by inhibiting Cd translocation, whereas it significantly increased Zn accumulation in shoots. This study confirms that although rhamnolipid could enhance accumulation of Cd in plants roots at low Ca supply, it is not suitable for Cd phytoextraction in contaminated soil environments where Ca concentrations in soil solution are orders of magnitude greater than those of Cd.

Keywords

Metals Phytoremediation Rhamnolipid Free ion activity model 

References

  1. Allen HE (1993) The significance of trace metal speciation for water, sediment and soil quality criteria and standards. Sci Total Environ 134:23–45CrossRefGoogle Scholar
  2. Allen HE, Hall RH, Brisbin TD (1980) Metal speciation. Effects on aquatic toxicity. Environ Sci Technol 14:441–443CrossRefGoogle Scholar
  3. Bell PF, Chaney RL, Angle JS (1991) Free metal activity and total metal concentrations as indices of micronutrient availability to barley [Hordeum vulgare (L.) Klages]. Plant Soil 130:51–62CrossRefGoogle Scholar
  4. Bell PF, McLaughlin MJ, Cozens G, Stevens DP, Owens G, South H (2003) Plant uptake of C-14-EDTA, C-14-citrate, and C-14-histidine from chelator-buffered and conventional hydroponic solutions. Plant Soil 253:311–319CrossRefGoogle Scholar
  5. Bell RW, Edwards DG, Asher CJ (1989) Effects of calcium supply on uptake of calcium and selected mineral nutrients by tropical food legumes in solution culture. Aust J Agric Res 40:1003–1013CrossRefGoogle Scholar
  6. Berkelaar EJ, Hale BA (2003) Cadmium accumulation by durum wheat roots in ligand-buffered hydroponic culture: uptake of Cd-ligand complexes or enhanced diffusion? Can J Bot 81:755–763CrossRefGoogle Scholar
  7. Campbell PGC (1995) Interactions between trace metals and aquatic organisms: a critique of the free ion activity model. In: Tessier A, Turner DR (eds) Metal speciation and bioavailability in aquatic systems, vol 3. Wiley, New York, pp. 45–102Google Scholar
  8. Chaudhry FM, Loneragan JF (1972) Zinc absorption by wheat seedlings: I. Inhibition by macronutrient ions in short-term experiments and its relevance to long-term zinc nutrition. Soil Sci Soc Am Proc 36:323–327CrossRefGoogle Scholar
  9. Checkai RT, Corey RB, Helmke PA (1987) Effects of ionic and complexed metal concentrations on plant uptake of cadmium and micronutrient metals from solution. Plant Soil 99:335–345CrossRefGoogle Scholar
  10. Chen YH, Li XD, Shen ZG (2004) Leaching and uptake of heavy metals by ten different species of plants during an EDTA-assisted phytoextraction process. Chemosphere 57:187–196CrossRefGoogle Scholar
  11. Collins RN, Merrington G, McLaughlin MJ, Knudsen C (2002) Uptake of intact zinc-ethylenediaminetetraacetic acid from soil is dependent on plant species and complex concentration. Environ Toxicol Chem 21:1940–1945Google Scholar
  12. Degryse F, Smolders E, Parker D (2006a) Metal complexes increase uptake of Zn and Cu by plants: implications for uptake and deficiency studies in chelator-buffered solutions. Plant Soil 289:171–185CrossRefGoogle Scholar
  13. Degryse F, Smolders E, Merckx R (2006b) Labile Cd complexes increase Cd availability to plants. Environ Sci Technol 40:830–836CrossRefGoogle Scholar
  14. Elgawhary SM, Lindsay WL, Kemper WD (1970) Effect of EDTA on the self-diffusion of zinc in aqueous solution and in soil. Soil Sci Soc Am Proc 34:66–69CrossRefGoogle Scholar
  15. Epelde L, Hernández-Allica J, Becerril JM, Blanco F, Garbisu C (2008) Effects of chelates on plants and soil microbial community: comparison of EDTA and EDDS for lead phytoextraction. Sci Total Environ 401(1–3):21–28CrossRefGoogle Scholar
  16. Epstein AL, Gussman CD, Blaylock MJ, Yermiyahu U, Huang JW, Kapulnik Y, Orser CS (1999) EDTA and Pb-EDTA accumulation in Brassica juncea grown in Pb-amended soil. Plant Soil 208:87–94CrossRefGoogle Scholar
  17. Fu GM, Allen HE, Cao Y (1992) The importance of humic acids to proton and cadmium binding in sediments. Environ Toxicol Chem 11:1363–1372CrossRefGoogle Scholar
  18. Grundon NJ, Robson AD, Lambert MJ, Snowball KA (1997) Nutrient deficiency and toxicity symptoms. In: Reuter DJ, Robinson JB, Dutkiewicz C (eds) Plant analysis: an interpretation manual. CSIRO Publishing, Australia, pp. 35–47Google Scholar
  19. Gunawardana B, Singhal N, Johnson A (2010) Amendments and their combined application for enhanced copper, cadmium, lead uptake by Lolium perenne. Plant Soil 329:283–294CrossRefGoogle Scholar
  20. Herman DC, Artiola JF, Miller RM (1995) Removal of cadmium, lead, and zinc from soil by a rhamnolipid biosurfactant. Environ Sci Technol 29:2280–2285CrossRefGoogle Scholar
  21. Huang JW, Chen J, Berti WR, Cunningham SD (1997) Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Technol 31:800–805CrossRefGoogle Scholar
  22. Jarvis SC, Jones JHP, Hopper MJ (1976) Cadmium uptake from solution by plants and its transport from roots to shoots. Plant Soil 44:179–191CrossRefGoogle Scholar
  23. Johnson A, Gunawardana B, Singhal N (2009) Amendments for enhancing copper uptake by Brassica juncea and Lolium perenne from solution. Int J Theor Phytoremediation 11:215–234CrossRefGoogle Scholar
  24. Jordan FL, Robbin-Abbott M, Maier RM, Glenn EP (2002) A comparison of chelator-facilitated metal uptake by a halophyte and a glycophyte. Environ Toxicol Chem 21:2698–2704Google Scholar
  25. Juwarkar AA, Nair A, Dubey KV, Singh SK, Devotta S (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68:1996–2002CrossRefGoogle Scholar
  26. Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213CrossRefGoogle Scholar
  27. Ławniczak Ł, Marecik R, Chrzanowski Ł (2013) Contributions of biosurfactants to natural or induced bioremediation. Appl Microbiol Biotechnol 97:2327–2339CrossRefGoogle Scholar
  28. Marecik R, Wojtera-Kwiczor J, Ławniczak Ł, Cyplik P, Szulc A, Piotrowska-Cyplik A, Chrzanowski Ł (2012) Rhamnolipid increase the phytotoxicity of diesel oil towards four common plant species in a terrestrial environment. Water Air Soil Pollut 223:4275–4282CrossRefGoogle Scholar
  29. McLaughlin MJ (2002) Bioavailability of metals to terrestrial plants. In: Allen HE (ed) Bioavailability of metals in terrestrial ecosystems. Influence of partitioning for bioavailability to invertebrates, microbes and plants. SETAC Press, Pensacola, FL, pp. 173–195Google Scholar
  30. McLaughlin MJ, Smolders E, Merckx R, Maes A (1997) Plant uptake of Cd and Zn in chelator-buffered nutrient solution depends on ligand type. In: Ando T (ed) Plant nutrition—for sustainable food production and environment. Kluwer Academic Publishers, Japan, pp. 113–118CrossRefGoogle Scholar
  31. McLaughlin MJ, Lambrechts RM, Smolders E, Smart MK (1998a) Effects of sulfate on cadmium uptake by Swiss chard: II. Effects due to sulfate addition to soil. Plant Soil 202:217–222CrossRefGoogle Scholar
  32. McLaughlin MJ, Andrew SJ, Smart MK, Smolders E (1998b) Effects of sulfate on cadmium uptake by Swiss chard: I. Effects of complexation and calcium competition in nutrient solutions. Plant Soil 202:211–216CrossRefGoogle Scholar
  33. Meers E, Ruttens A, Hopgood MJ, Samson D, Tack FMG (2005) Comparison of EDTA and EDDS as potential soil amendments for enhanced phytoextraction of heavy metals. Chemosphere 58:1011–1022CrossRefGoogle Scholar
  34. Mulligan CN (2005) Environmental applications for biosurfactants. Environ Pollut 133:183–198CrossRefGoogle Scholar
  35. Mulligan CN, Yong RN, Gibbs BF (2001) Heavy metal removal from sediments by biosurfactants. J Hazard Mater 85:111–125CrossRefGoogle Scholar
  36. Nolan AL, McLaughlin MJ, Mason SD (2003) Chemical speciation of Zn, Cd, Cu and Pb in pore waters of agricultural and contaminated soils using Donnan dialysis. Environ Sci Technol 37:90–98CrossRefGoogle Scholar
  37. Noraho N, Gaur JP (1995) Effect of cations, including heavy metals, on cadmium uptake by Lemna polyrhiza L. Biometals 8:95–98CrossRefGoogle Scholar
  38. Nowack B, Schulin R, Robinson BH (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40:5225–5232CrossRefGoogle Scholar
  39. Ochoa-Loza FJ, Artiola JF, Maier RM (2001) Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30:479–485CrossRefGoogle Scholar
  40. Pavan MA, Bingham FT (1982) Toxicity of aluminum to coffee seedlings grown in nutrient solution. Soil Sci Soc Am J 46:993–997CrossRefGoogle Scholar
  41. Phinney JT, Bruland KW (1994) Uptake of lipophilic organic Cu, Cd, and Pb complexes in the coastal diatom Thalassiosira weissflogii. Environ Sci Technol 28:1781–1790CrossRefGoogle Scholar
  42. Prokop Z, Cupr P, Zlevorova-Zlamalikova V, Komarek J, Dusek L, Holoubek I (2003) Mobility, bioavailability, and toxic effects of cadmium in soil samples. Environ Res 91:119–126CrossRefGoogle Scholar
  43. Sauvé S, Dumestre A, McBride M, Hendershot W (1998) Derivation of soil quality criteria using predicted chemical speciation of Pb2+ and Cu2+. Environ Toxicol Chem 17:1481–1489CrossRefGoogle Scholar
  44. Smolders E, McLaughlin MJ (1996) Effect of Cl on Cd uptake by Swiss chard in nutrient solutions. Plant Soil 179:54–64CrossRefGoogle Scholar
  45. Stacey SP, McLaughlin MJ, Cakmak I, Hetitiarachchi GM, Scheckel KG, Karkkainen M (2008) Root uptake of lipophilic zinc-rhamnolipid complexes. J Agric Food Chem 56:2112–2117CrossRefGoogle Scholar
  46. Tan H, Champion JT, Artiola JF, Brusseau ML, Miller RM (1994) Complexation of cadmium by a rhamnolipid biosurfactant. Environ Sci Technol 28:2402–2406CrossRefGoogle Scholar
  47. Tandy S, Schulin R, Nowack B (2006) The influence of EDDS on the uptake of heavy metals in hydroponically grown sunflowers. Chemosphere 62:1454–1463CrossRefGoogle Scholar
  48. Tyler LD, McBride MB (1982) Influence of Ca, pH and humic acid on Cd uptake. Plant Soil 64:259–262CrossRefGoogle Scholar
  49. Vassil AD, Kapulnik Y, Raskin I, Salt DE (1998) The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol 117:447–453CrossRefGoogle Scholar
  50. Wagatsuma T, Kaneko M, Hayasaka Y (1987) Destruction process of plant-root cells by aluminum. Soil Sci Plant Nutr 33:161–175CrossRefGoogle Scholar
  51. Wen J, Stacey SP, McLaughlin MJ, Kirby JK (2009) Biodegradation of rhamnolipid, EDTA and citric acid in cadmium and zinc contaminated soils. Soil Biol Biochem 41:2214–2221CrossRefGoogle Scholar
  52. Wen J, McLaughlin MJ, Stacey SP, Kirby JK (2010) Is rhamnolipid biosurfactant useful in cadmium phytoextraction? J Soils Sediments 10:1289–1299CrossRefGoogle Scholar
  53. Zaier H, Ghnaya T, Rejeb KB, Lakhdar A, Rejeb S, Jemal F (2010) Effects of EDTA on phytoextraction of heavy metals (Zn, Mn and Pb) from sludge-amended soil with Brassica napus. Bioresour Technol 101(11):3978–3983CrossRefGoogle Scholar
  54. Zarcinas BA, McLaughlin MJ, Smart MK (1996) The effect of acid digestion technique on the performance of nebulisation systems used in inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal 27:1331–1354CrossRefGoogle Scholar
  55. Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543CrossRefGoogle Scholar
  56. Zhao SL, Lian F, Duo L (2011) EDTA-assisted phytoextraction of heavy metals by turfgrass from municipal solid waste using permeable barriers and associated potential leaching risk. Bioresour Technol 102(2):621–626CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Jia Wen
    • 1
    • 2
  • Mike J. McLaughlin
    • 1
    • 3
  • Samuel P. Stacey
    • 1
    • 4
  • Jason K. Kirby
    • 3
  1. 1.Soil Science, School of Agriculture, Food and WineThe University of AdelaideGlen OsmondAustralia
  2. 2.College of Environmental Science and EngineeringHunan UniversityChangshaPeople’s Republic of China
  3. 3.CSIRO Land and Water, Agricultural Sustainable Flagship, Environmental Biogeochemistry ProgramUrrbraeAustralia
  4. 4.Everris Australia Pty LtdBella VistaAustralia

Personalised recommendations