Abstract
The demand for rare earth elements has increased dramatically in recent years because of their numerous industrial applications, and considerable research efforts have consequently been directed toward recycling these materials. The accumulation of metals in microorganisms is a low-cost and environmentally friendly method for the recovery of metals present in the environment at low levels. Numerous metals, including rare earth elements, can be readily dissolved in aqueous acid, but the efficiency of metal biosorption is usually decreased under the acidic conditions. In this report, we have investigated the use of the sulfothermophilic red alga Galdieria sulphuraria for the recovery of metals, with particular emphasis on the recovery of rare earth metals. Of the five different growth conditions investigated where G. sulphuraria could undergo an adaptation process, Nd(III), Dy(III), and Cu(II) were efficiently recovered from a solution containing a mixture of different metals under semi-anaerobic heterotrophic condition at a pH of 2.5. G. sulphuraria also recovered Nd(III), Dy(III), La(III), and Cu(II) with greater than 90 % efficiency at a concentration of 0.5 ppm. The efficiency remained unchanged at pH values in the range of 1.5–2.5. Furthermore, at pH values in the range of 1.0–1.5, the lanthanoid ions were collected much more efficiently into the cell fractions than Cu(II) and therefore successfully separated from the Cu(II) dissolved in the aqueous acid. Microscope observation of the cells using alizarin red suggested that the metals were accumulating inside of the cells. Experiments using dead cells suggested that this phenomenon was a biological process involving specific activities within the cells.
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References
Ahlf W (1988) Recovery of metals from acid waste water by Cyanidium caldarium. Appl Microbiol Biotechnol 28:512–513
Allen MB (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Microbiol 32:270–277
Andrès Y, Texier AC, Cloirec PL (2003) Rare earth elements removal by micorobial biosorption: a review. Environ Technol 24:1367–1375
Ascione R, Southwick W, Fresco JR (1966) Laboratory culturing of thermophilic alga at high temperature. Science 12:752–755
Boyanov MI, Kelly SD, Kemner KM, Bunker BA, Fein JB, Fowle DA (2003) Adsorption of cadmium to Bacillus subtils bacterial cell walls: a pH-dependent X-ray adsorption fine structure spectroscopy study. Geochim Cosmochim Acta 67:3299–3311
Buchler JW (1997) Transition metal and rare earth porphyrin aggregates. In: Trautwein A (eds) Bioinorganic chemistry: transition metals in biology and their coordination chemistry. Deutsche Forschungsgemeinschaft, pp 570–584
Cordero B, Lodeiro P, Herrero R, Sastre de Vicente ME (2004) Biosorption of cadmium by Fucus spiralis. Environ Chem 1:180–187
Fukuda I (1958) Physiological studies on a thermophilic blue green alga, Cyanidium caldarium Geitler. Bot Mag Tokyo 71:79–86
Gorss W, Schnarrenberger C (1995) Heterotrophic growth of two strains of the acido-thermophilic red alga, Galdieria sulphuraria. Plant Cell Physiol 36:633–638
Graverholt OS, Eriksen NT (2007) Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Appl Microbiol Biotechnol 77:69–75
Güzel Y, Rainer M, Mirza MR, Messner CB, Bonn GK (2013) Highly selective recovery of phosphopeptides using trypsin-assisted digestion of precipitated lanthanide-phosphoprotein complexes. Analyst 138:2897–2905
Hosomomi Y, Baba Y, Kubota F, Kamiya N, Goto M (2013) Biosorption of rare earth elements by Escherichia coli. J Chem Eng Jpn 46:450–454
Jiang M, Ohnuki T, Kozai N, Tanaka K, Suzuki Y, Sakamoto F, Kamiishi E, Utusnomiya S (2010) The Biological nano-mineralization of Ce phosphate by Saccharomyces cerevisiae. Chem Geol 277:61–69
Karavaiko GI, Kareva AS, Avakian ZA, Zakharova VI, Korenevsky AA (1996) Biosorption of scandium and yttrium from solutions. Biotechnol Lett 18:1291–1296
Küpper H, Küpper FC, Spiller M (2006) [Heavy metal]-chlorophylls formed in vivo during heavy metal stress and degradation products formed during digestion, extraction and storage of plant material. In: Grimm R, Rüdiger PW, Scheer H (eds) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Academic Publishers, Dordecht, pp 67–77
Kuroda K, Ueda M (2010) Engineering of microorganisms towards recovery of rare metal ions. Appl Microbiol Biotechnol 87:53–60
Kuyucak N, Volesky B (1989) Accumulation of cobalt by marine alga. Biotechnol Bioeng 33:809–814
Lafraie MA, Betz A (1985) Anaerobic fermentation in Cyanidium caldarium. Planta 163:38–42
Matsunaga T, Takeyama H, Nakao T, Yamazawa A (1999) Screening of marine microalgae for bioremediation of cadmium-polluted seawater. J Biotechnol 70:33–38
Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152
Mehta SK, Tripathi BN, Gaur JP (2002) Enhanced sorption of Cu2+ and Ni2+ by acid-pretreated Chlorella vulgaris from single and binary metal solutions. J Appl Phycol 14:267–273
Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45:667–671
Nagasaka S, Nishizawa NK, Watanabe T, Mori S, Yoshimura E (2003) Evidence that electron-dense bodies in Cyanidium caldarium have an iron-storage role. Biometals 16:465–470
Nagasaka S, Nishizawa NK, Mori S, Yoshimura E (2004) Metal metabolism in the red alga Cyanidium caldarium and its relationship to metal tolerance. Biometals 17:177–181
Oesterhelt C, Schmälzlin E, Schmitt JM, Lokstein H (2007) Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria. Plant J 51:500–511
Schönknecht G, Schönknecht G, Chen WH, Ternes CM, Barbier GG, Shrestha RP, Stanke M, Bräutigam A, Baker BJ, Banfield JF, Garavito RM, Carr K, Wilkerson C, Rensing SA, Gagneul D, Dickenson NE, Oesterhelt C, Lercher MJ, Weber AP (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210
Seckbach J, Baker FA (1970) Algae thrive under pure CO2. Nature 227:744–745
Takahashi Y, Châtellier X, Hattori KH, Kato K, Fortin D (2005) Adsorption of rare earth elements onto bacterial cell walls and its implification for REE sorption onto natural microbial mats. Chem Geol 219:53–67
Texier AC, Andrès Y, Cloirec PL (1999) Selective biosorption of lanthanide (La, Eu, Yb) ions by Pseudomonas aeruginosa. Environ Sci Technol 33:489–495
Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226
Wood JM, Wang HK (1983) Microbial resistance to heavy metals. Environ Sci Technol 17:582–590
Yoshimura E, Nagasaka S, Sato Y, Satake K, Mori S (1999) Extraordinary high aluminium tolerance of the acidic themophilic alga, Cyanidium caldarium. Soil Sci Plant Nutr 45(3):721-724
Acknowledgments
We would like to thank the Chemical Analysis Division of the University of Tsukuba for their helpful support with the ICP-MS measurements. This study was supported by PRESTO (to A.M.) from the Japan Science and Technology Agency, as well as a research grant from the Chemical Analysis Division of the University of Tsukuba (to A.M.).
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Minoda, A., Sawada, H., Suzuki, S. et al. Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid. Appl Microbiol Biotechnol 99, 1513–1519 (2015). https://doi.org/10.1007/s00253-014-6070-3
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DOI: https://doi.org/10.1007/s00253-014-6070-3