Abstract
Purpose
Successful chelant-assisted phytoextraction requires application of an eco-friendly metal-complexing agent which enhances metal uptake but does not pose a significant risk of off-site movement of metals. Rhamnolipid biosurfactant has been used to enhance cadmium (Cd) removal from contaminated soil by washing. It has a strong affinity for Cd compared to some other hazardous metals, suggesting that rhamnolipid could be useful in Cd phytoextraction. This study investigated the potential use of rhamnolipid to enhance Cd phytoextraction.
Materials and methods
Adsorption patterns of rhamnolipid in soils were investigated by batch adsorption experiments. Hydrophobicity of rhamnolipid–metal complexes were determined by assessing partitioning in an octanol/water system. Phytotoxicity of rhamnolipid to maize (Zea mays) and chelant-assisted phytoextraction efficiency of maize and sunflower (Helianthus annuus) were determined in pot experiments.
Results and discussion
The results showed that rhamnolipid was prone to adsorb strongly to soil at low application rates (0.1–1.7 mM) possibly due to its hydrophobic interactions with soil organic matter, hence reducing its capacity to complex and transport metals to plant roots. Rhamnolipid mobility increased (i.e. decreased soil phase partitioning) at elevated concentrations (∼4.4 mM), which increased soil solution Cd concentrations possibly due to its reduced hydrophobic nature. The use of rhamnolipid at concentrations >4.4 mM severely reduced maize biomass yield, reducing the potential for chelant-assisted phytoextraction. At lower concentrations of rhamnolipid (0.02–1.4 mmol/kg), there was insignificant enhancement of Cd accumulation by plant (Z. mays and H. annuus) shoots, likely through strong retention of the chelant (or Cd-associated rhamnolipid) on soil surfaces.
Conclusions
High rates of rhamnolipid addition to soils in this study caused severe phytotoxicity to maize and sunflower. Lower rates of rhamnolpid addition to soils in this study did not improve Cd accumulation by plants. Therefore, the sorption of rhamnolipid (or Cd-associated rhamnolipid) to soils, along with the phytotoxicity and phytoextraction results, suggests that neither low nor high concentrations of rhamnolipid are likely to consistently assist Cd phytoextraction using maize or sunflower.
Similar content being viewed by others
References
Alkorta I, Hernández-Allica J, Becerril JM, Amezaga I, Albizu I, Onaindia M, Garbisu C (2004) Chelate-enhanced phytoremediation of soils polluted with heavy metals. Rev Environ Sci Biotechnol 3:55–70
Asami T, Kubota M, Orikasa K (1995) Distribution of different fractions of cadmium, zinc, lead, and copper in unpolluted and polluted soils. Water Air Soil Pollut 83:187–194
Aşçi Y, Nurbas M, Acikel YS (2007) Sorption of Cd(II) onto kaolin as a soil component and desorption of Cd(II) from kaolin using rhamnolipid biosurfactant. J Hazard Mater 139:50–56
Aşçi Y, Nurbas M, Acikel YS (2008) Removal of zinc ions from a soil component Na-feldspar by a rhamnolipid biosurfactant. Desalination 223:361–365
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 253:311–319
Bruemmer G, Gerth J, Tiller KG (1988) Reaction kinetics of the adsorption and desorption of nickel, zinc and cadmium by geothite. I. Adsorption and diffusion of metals. Eur J Soil Sci 39:37–52
Champion JT, Gilkey JC, Lamparski H, Retterer J, Miller RM (1995) Electron-microscopy of rhamnolipid (biosurfactant) morphology—effects of pH, cadmium, and octadecane. J Colloid Interface Sci 170:569–574
Chandrasekaran EV, BeMiller JN (1980) Constituent analysis of glycosaminoglycans. In: Whistler RL, Wolfrom ML (eds) Methods in carbohydrate chemistry. Academic, New York, pp 89–96
Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284
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 57:187–196
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 21:1940–1945
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 34:66–69
Guo YP, Hu YY, Gu RR, Lin H (2009) Characterization and micellization of rhamnolipidic fractions and crude extracts produced by Pseudomonas aeruginosa mutant MIG-N146. J Colloid Interface Sci 331:356–363
Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420
Herman DC, Artiola JF, Miller RM (1995) Removal of cadmium, lead, and zinc from soil by a rhamnolipid biosurfactant. Environ Sci Technol 29:2280–2285
Johnson A, Gunawardana B, Singhal N (2009) Amendments for enhancing copper uptake by Brassica juncea and Lolium perenne from solution. Int J Phytoremediation 11:215–234
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 21:2698–2704
Juwarkar AA, Nair A, Dubey KV, Singh SK, Devotta S (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68:1996–2002
Kos B, Lestan D (2004) Chelator induced phytoextraction and in situ soil washing of Cu. Environ Pollut 132:333–339
Laurie SH, Tancock NP, McGrath SP, Sanders JR (1991a) Influence of complexation on the uptake by plants of iron, manganese, copper and zinc. 1. Effect of EDTA in a multi-metal and computer-simulation study. J Exp Bot 42:509–513
Laurie SH, Tancock NP, McGrath SP, Sanders JR (1991b) Influence of complexation on the uptake by plants of iron, manganese, copper and zinc. 2. Effect of DTPA in a multi-metal and computer-simulation study. J Exp Bot 42:515–519
Luo CL, Shen ZG, Li XD (2005) Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59:1–11
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, Pensacola, pp 173–195
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, Japan, pp 113–118
McLaughlin MJ, Andrew SJ, Smart MK, Smolders E (1998) Effects of sulfate on cadmium uptake by Swiss chard: I. Effects of complexation and calcium competition in nutrient solutions. Plant Soil 202:211–216
Means JL, Kucak T, Crerar DA (1980) Relative degradation rates of NTA, EDTA and DTPA and environmental implications. Environ Pollut B Chem Phys 1:45–60
Mulligan CN (2005) Environmental applications for biosurfactants. Environ Pollut 133:183–198
Mulligan CN (2009) Recent advances in the environmental applications of biosurfactants. Curr Opin Colloid Interface Sci 14:372–378
Noordman WH, Brusseau ML, Janssen DB (2000) Adsorption of a multicomponent rhamnolipid surfactant to soil. Environ Sci Technol 34:832–838
Nowack B, Schulin R, Robinson BH (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40:5225–5232
Ochoa-Loza FJ, Artiola JF, Maier RM (2001) Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30:479–485
Ochoa-Loza FJ, Noordman WH, Janssen DB, Brusseau ML, Maier RM (2007) Effect of clays, metal oxides, and organic matter on rhamnolipid biosurfactant sorption by soil. Chemosphere 66:1634–1642
Pritsa TS, Fotiadis EA, Lolas PC (2008) Corn tolerance to atrazine and cadmium and sunflower to cadmium in soil and hydroponic culture. Commun Soil Sci Plant Anal 39:1168–1182
Rengel Z, Wheal MS (1997) Kinetic parameters of Zn uptake by wheat are affected by the herbicide chlorsulfuron. J Exp Bot 48:935–941
Römkens P, Bouwman L, Japenga J, Draaisma C (2002) Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environ Pollut 116:109–121
Sánchez M, Aranda FJ, Espuny MJ, Marqués A, Teruel JA, Manresa Á, Ortiz A (2007) Aggregation behaviour of a dirhamnolipid biosurfactant secreted by Pseudomonas aeruginosa in aqueous media. J Colloid Interface Sci 307:246–253
Shin K, Kim K, Kim J, Lee K, Han S (2008) Rhamnolipid morphology and phenanthrene solubility at different pH values. J Environ Qual 37:509–514
Stacey SP, McLaughlin MJ, Cakmak I, Hetitiarachchi GM, Scheckel KG, Karkkainen M (2008) Root uptake of lipophilic zinc–rhamnolipid complexes. J Agric Food Chem 56:2112–2117
Tan H, Champion JT, Artiola JF, Brusseau ML, Miller RM (1994) Complexation of cadmium by a rhamnolipid biosurfactant. Environ Sci Technol 28:2402–2406
Tandy S, Schulin R, Nowack B (2006) The influence of EDDS on the uptake of heavy metals in hydroponically grown sunflowers. Chemosphere 62:1454–1463
Torrens JL, Herman DC, Miller-Maier RM (1998) Biosurfactant (rhamnolipid) sorption and the impact on rhamnolipid-facilitated removal of cadmium from various soils under saturated flow conditions. Environ Sci Technol 32:776–781
Trapp S (2002) Dynamic root uptake model for neutral lipophilic organics. Environ Toxicol Chem 21:203–206
Turan M, Angin I (2004) Organic chelate assisted phytoextraction of B, Cd, Mo and Pb from contaminated soils using two agricultural crop species. Acta Agric Scand Sect B–Soil Plant Sci 54:221–231
Wang SL, Mulligan CN (2004) Rhamnolipid foam enhanced remediation of cadmium and nickel contaminated soil. Water Air Soil Pollut 157:315–330
Wen J, Stacey S, McLaughlin M, Kriby J (2009) Biodegradation of rhamnolipid, EDTA and citric acid in cadmium and zinc contaminated soils. Soil Biol Biochem 41:2214–2221
Zhang YM, Miller RM (1992) Enhanced octadecane dispersion and biodegradation by a pseudomonas rhamnolipid surfactant (biosurfactant). Appl Environ Microbiol 58:3276–3282
Acknowledgements
We thank Michelle Smart and Claire Wright for technical support in ICP-OES and ICP-MS analysis and Margaret Cargill for assistance with manuscript preparation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Willie Peijnenburg
Rights and permissions
About this article
Cite this article
Wen, J., McLaughlin, M.J., Stacey, S.P. et al. Is rhamnolipid biosurfactant useful in cadmium phytoextraction?. J Soils Sediments 10, 1289–1299 (2010). https://doi.org/10.1007/s11368-010-0229-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-010-0229-z