Abstract
The pressure to develop environmentally friendly recycling methods for rare earth elements (REEs) is increasing. The unicellular red alga Galdieria phlegrea was used as an experimental organism to examine the bioaccumulation of REEs from luminophores, the e-waste from lighting technologies. Algal cells were cultured mixotrophically in a liquid medium with the addition of glycerol as a source of carbon. Luminophores from two different sources (energy saving light bulbs—CFL, fluorescence lamps—FL) were added to the medium in the form of a powder. Cell number was monitored to follow the growth of the algal culture, and pigments were extracted and measured spectrophotometrically. The content of individual REEs in the luminophores and the resulting algal biomass were determined using inductively coupled plasma mass spectrometry (ICP-MS). Total REEs were twofold higher in luminophores from CFL than from FL. The most abundant element in both preparations of luminophores was yttrium, representing about 90% w/w. Growth of cultures incubated in the presence of CFL and FL luminophores was enhanced, but more so in the case of FL. The total level of REEs that accumulated in biomass differed with the type and concentration of luminophore used. The most abundant element that accumulated in algal biomass was yttrium, followed by europium and lanthanum. The chlorophyll content of the algae was enhanced markedly by luminophore treatment, but to a greater extent with luminophores from CFL. This study shows that Galdieria phlegrea can grow in the presence of luminophores and can accumulate REEs. The enriched biomass is a promising template for further applications in biotechnology.
Graphic Abstract
Similar content being viewed by others
Statement of Novelty
The risk to global supplies of rare earth elements for electronic devices and other modern technologies has led to the emergence of recycling methods from secondary sources. As the current physicochemical recycling techniques are usually expensive and environmentally unfriendly, there is an effort to develop some biological alternative. Here, we provide a novel application of the extremophilic unicellular red alga Galdieria in accumulating rare earth elements from waste luminophores collected from energy saving bulbs and fluorescent lamps. The alga is able to grow in a highly acidic environment (pH 2), which enables its use even in acidic extracts of rare earth elements from e-waste. The cultivation of Galdieria was conducted under mixotrophic or heterotrophic regimes using industrial waste glycerol as a source of carbon.
Introduction
Rare earth elements (REEs) form a group of chemical elements including scandium (Sc), yttrium (Y), and a series of 15 lanthanides. They exhibit very similar physical and chemical properties [1] and their unique magnetic and catalytic properties make them appropriate for exploitation in almost all electronic and clean energy technologies. In addition to the industrial sector, REEs are also utilized in agriculture as fertilizers, growth enhancers of animals or in aquaculture [2,3,4,5,6].
Luminophores possess light emitting and/or light conversion properties for which they are widely used in color display fluorescent lamps, television screens, computer monitor screens etc. All these products provide an enormous amount of e-waste. However, to use these waste products as a source of REEs, it is necessary to consider that these sources can differ greatly in their individual REE contents, as well as their ratios to each other.
The availability of REE resources in China, as the world’s main producer, is becoming limited and the depletion of other natural resources is possible. Therefore, REEs are considered as critical raw materials because of their high supply risk and economic importance [7]. With increasing demand, the importance of recycling REEs from industrial waste has risen. Research has recently focused on environmentally-friendly technologies of metal recovery from secondary resources [8, 9] including biological methods such as biosorption, bioelectrochemical systems, bioleaching and biomineralization [10, 11].
The end-of-life products considered as a rich secondary source of REEs include waste luminophores, particularly from fluorescent lamps and LEDs. For example, luminophores from discarded tubular lights comprise about 34% of the global levels of REEs. The life cycle assessment study of REE recovery from waste luminophores showed that the most environmentally beneficial scenario was when REEs were recycled from final disposal, substituting for virgin REEs [12].
REEs from e-waste can be recovered by chemical approaches such as leaching, but these methods are relatively expensive and non-ecological [13, 14]. The recovery of REEs from e-waste through biological processes may offer alternatives and could supplement physicochemical techniques for recycling. Bioleaching of waste luminophores by Gluconabacter oxidans [15], Zygosaccharomyces lentus, Kombucha culture [16] or Acidithiobacillus ferrooxidans [17] have already been described. The green alga Desmodesmus quadricauda was used for bioaccumulation of REEs from waste luminophores [18].
However, studies of REE recovery by algae or cyanobacteria are rare. The red alga Galdieria sulphuraria and the macroalga Gracillaria gracilis were effectively used to recover REEs from waste water [19, 20]. Biosorption of single REEs in biomass of both microscopic and macroscopic algal and blue-green algal species was reported [21], reviewed by [22]. The cyanobacterium Anabaena was able to enrich dissolved europium, samarium and neodymium and formed europium particles inside the cells [23]. Biomining of REEs from red mud, a byproduct of alumina production, using 3 species of green microalgae, was tested successfully [24]. The effects of REEs on algae were also studied to evaluate their potential in bioremediation or recycling [25,26,27,28].
Considering algal species that could be used for recycling or bio-mining of REEs from various sources, under conditions often not ideal for the growth of different organisms, we have chosen as a promising organism, the extremophilic unicellular red alga Galdieria [29]. The species Galdieria occurs in hot, acidic sulfur springs with temperatures up to 56 °C and pH values between 0.05 and 3 [30]. It can grow photoautotrophically, mixotrophically or heterotrophically in the dark [31]. Under heterotrophic conditions, this species grew to an enormous cell concentration (up to 100 g/L) in a growth medium where the concentration of glucose was increased from 50 to 500 g/L. The nitrogen source, (NH4)2SO4, was added in concentrations from 11 to 110 g/L [32]. Galdieria can grow heterotrophically on more than 50 different carbon sources [33, 34]. For most algal species, organic sources of carbon and energy for heterotrophic growth are limited mostly to glucose or acetate and, to a lesser extent, some other mono-saccharides. From organic sources effectively used by Galdieria, glycerol seems to be the best choice as a source of carbon and energy because it is produced industrially in enormous amounts as an undesirable byproduct during the production of biofuels from rape [35].
The aim of this study was to examine the ability of the red alga Galdieria phlegrea to accumulate REEs from waste luminophores obtained from fluorescence lamps and energy saving bulbs containing a high concentration of REEs. In order to examine bio-absorption capacity and physiological effects of REEs, G. phlegrea was cultivated mixotrophically in the presence of different types and concentrations of waste luminophores. The concentration and composition of REEs accumulated in algal biomass were determined using inductively coupled plasma mass spectrometry (ICP-MS), and the potential to use red algae for bioaccumulation of REEs from waste luminophores was evaluated.
Material and Methods
Experimental Organism and Culturing
The unicellular red alga Galdieria phlegrea, strain Nr. 613 (Rhodophyta) was obtained from the Algal Collection of Dipartimento delle Scienze Biologiche, Section of Plant Biology, University “Federico II” of Naples, Italy (https://www.acuf.net/index.php?lang=en). Cultures were grown in glass cylinders of inner diameter 36 mm, height 500 mm and volume 300 mL. Cylinders were placed in a thermostatic water bath and illuminated by a panel of dimmable fluorescent lamps (OSRAM DULUX L55 W/950 Daylight, Milano, Italy) allowing adjustment of the incident light intensity from 16 to 780 µmol/m2/s1. Algal suspensions in the cylinders were supplied with a gas mixture of air and CO2 (2% v/v), at a flow rate of 15 L/h. The experiments were carried out in a batch culture regime, at 39 °C and incident light intensity of 150 µmol/m2/s1. The photobioreactors were operated in triplicate.
The cultures were grown in modified Galdieria-nutrient medium, pH 4 [36] with the following final composition of macroelements (g/L): 1.31 (NH4)2SO4, 0.27 KH2PO4, 0.25 MgSO4·7H2O, 0.02 C10H12O8N2NaFe, 0.14 CaCl2·2H2O, and microelements diluted 500 × from the stock solution (mg/L): 31 H3BO3, 1.25 CuSO4·5H2O, 22.3 Mn SO4·4H2O, 0.88 (NH4)6Mo7O24·4H2O, 2.87 ZnSO4·7H2O, 1.46 Co(NO3)2·6H2O, 0.014 V2O4(SO4)3·16H2O, 0.3 Na2NO4·7H2O, 1.19 KBr, 0.83 KI, 0.91 CdCl2, 0.78 NiSO4, 0.12 CrO3, 4.74 Al2(SO4)3K2SO4·24H2O (all chemicals from Penta, Chrudim, Czech Republic) in distilled water, autoclaved for 20 min. Glycerol (to a final concentration of 1% v/v) (Penta, Chrudim, Czech Republic) was added as a source of energy and carbon for heterotrophic and mixotrophic cultivation. A concentration of 1% was found to be optimal for Galderia growth and was sufficient to support exponential growth for about 5 days (dry matter from 0.3 to about 5 mg/mL). Higher concentrations had a limiting effect on growth rate (not shown in figures). Therefore, this time interval for experiments to study the effect of REEs was used. To allow for further mixotrophic or heterotrophic growth, repeated doses of glycerol were added to the culture (see below in “Results and Discussion”, Fig. 1).
Biomass was harvested by centrifugation (ROTINA 380R, HETTICH, Tuttlingen, Germany) at 5 000 rpm for 10 min, washed 4 times with distilled H2O, frozen at − 80 °C and freeze-dried (CoolSafe 95-15Pro, Labogene, Lillerod, Denmark).
Luminophore Treatment
Luminophores from two sources of electrical waste: energy saving bulbs (CFL) and fluorescence lamps (FL) provided by the company RECYKLACE EKOVUK a.s. (Příbram, Czech Republic), were applied in a powder form and added to the nutrient medium at concentrations of 100, 200 and 300 mg/L. The average sizes of unresolved particles of CFL and FL luminophores were 25 µm3 and 21 µm3, respectively.
Growth Evaluation
Growth of cultures was expressed as the number of algal cells/mL, determined by counting cells under transmitted light in a Bürker counting chamber (Meopta, Přerov, Czech Republic) using a BX51 microscope (Olympus, Tokyo, Japan).
Dry Matter Determination
Dry matter was determined from 5 mL of algal suspension centrifuged at 3000 rpm for 5 min in dried and pre-weighed 5 mL Eppendorf tubes. The pellet was dried at 105 °C for 12 h and weighed on a Sartorius 1601 MPB analytical balance. Data in graphs are presented as means ± SD of at least 3 experiments.
Pigment Quantification
A 10 mL sample of suspension was centrifuged at 4000 rpm for 5 min. One mL of phosphate buffer (0.1 M KH2PO4: 0.1 M Na2HPO4·12H2O, 1:9; pH 7.7) and 10 µg of MgCO3 were added to the pellet. The pellet was vortexed for 5 min with 500 µL of 0.75–1.00 mm glass beads (P-LAB, Prague, Czech Republic) to break the cell walls. For the extraction, 4 mL of 100% acetone were added, mixed well and centrifuged at 4000 rpm for 5 min. The supernatant was transferred to a calibrated tube with a stopper and placed in a dark block. To the remaining pellet, 4 mL of 80% acetone were added, mixed and centrifuged at 4000 rpm for 5 min. The supernatant was transferred to the calibrated tube in the dark block with the supernatant from the first step of the extraction. This volume was increased to 10 mL using 80% acetone. The absorbance of the solution was measured in a UV-1800 spectrophotometer, Shimadzu Corporation (Kyoto, Japan) at 750, 664, 647, 470 and 450 nm. The content of chlorophyll a and carotenes were calculated as: C(Chl a) = 12.25 A664 − 2.79 A647 (µg/mL) and C(car) = ((1000 A470) − (1.82 C(Chl a))/198 (µg/mL) [37]. All chemicals were supplied by Penta (Chrudim, Czech Republic).
Quantitative Analysis of REE Content by ICP-MS
Samples of luminophores and algal biomass were digested with 67% HNO3 and 30% H2O2 (Merck, Suprapure) in a PTFE microwave oven (MLS1200 MEGA, Gemini bv, Apeldoorn, Netherland) at 250–600 W for 20 min. ICP-MS measurements were performed using an Elan DRC-e (Perkin Elmer, Concord, ON, Canada) equipped with a concentric PTFE nebulizer and cyclonic spray chamber. Samples were passed through a 0.45 µm nylon syringe filter (Millipore, Molsheim, France) and diluted 1:10 with distilled water. Values were expressed as milligrams per gram of dry matter (mg/g) [25].
Results and Discussion
Composition of Luminophores
For the present experiments, luminophores from two different sources of energy saving bulbs (CFL) and fluorescent lamps (FL) were chosen, because they contain a powerful red-emitting luminescent material, yttrium oxide, supplemented with a few percent of trivalent europium. The sources chosen had the same composition of individual REEs in slightly different ratios, but differed substantially in the total content of REEs (mg/g). This was more than twice as high in luminophores from energy saving bulbs (CFL) (196.41 mg/g) than from fluorescent lamps (FL) (87.00 mg/g) (sum in Table 1). The quantitative difference in total REE content reflects the different origins of the luminophores.
Individual REEs were quantified by ICP-MS. Yttrium was found to be the most abundant element in both types of luminophores, representing 90.96% and 89.20% of all REEs contained in CFL and FL luminophores, respectively (Table 1). Yttrium was followed by Eu (5.77 and 6.42% for CFL and FL respectively). Several other REEs (La, Ce, Gd and Tb) were also present in both luminophores but at very low values that varied from 1.60 to 0.48% (see values for La, Ce, Gd and Tb in Table 1).
The composition and content of individual REEs found in CFL and FL luminophores differed substantially from those found in other e-waste sources [18]. For example, yttrium was not found in luminophores from LCD monitors supplied either in powder form, where the most frequent REEs were Eu (61%) followed by lanthanum (17%), or in a HNO3 extract where the most frequent was neodymium (about 89%) [24], which was not found in the luminophores tested in this work. If being considered for any biotechnological application, the composition of REEs in possible sources should therefore be taken into account for any given application.
Mixotrophic and Heterotrophic Growth with Glycerol as a Source of Carbon and Energy
The experiments were carried out in a batch culture regime for 5 days (see subchapter “Experimental Organism and Culturing”).
Growth of G. phlegrea in the presence of glycerol was tested under both heterotrophic and mixotrophic conditions and compared with autotrophic cultivation (Fig. 1). Cultures grew in the presence of glycerol, both in light and dark, much faster than under autotrophic conditions and to extremely high cell concentrations. All cultures started to grow at an initial dry matter level of 0.34 mg/mL. The autotrophically grown culture increased its dry matter to 5.2 mg/mL (multiplied 16×, in 4 doublings, 24). During the same time interval, the heterotrophically and mixotrophically grown cultures attained dry matter of 47.7 and 56.3 mg/mL respectively, (multiplied 140 × and 160×—more than 7 doublings, 27) (Fig. 1). Such cell densities cannot be attained under autotrophic conditions because the mean irradiance decreases exponentially with increasing cell density due to the shadowing effect of cells. In dense cultures, only a very thin layer of cells in suspension is illuminated, while most of the cells in the population are practically in the dark. In autotrophic cultures, energy supplied only by light was less efficient and carbon had to be supplied in the form of CO2. The main advantage of heterotrophic growth with glycerol lies in the possibility that large scale cultivation may be possible in commercially produced bioreactors for biotechnological purposes, independent of the local climate, both from the point of view of outdoor temperature and varying levels of sunlight.
Accumulation of Rare Earth Elements in Biomass
To determine the content and composition of REEs absorbed by algal cells from nutrient medium, the algal biomass was analyzed by ICP-MS. Algal cultures grown in the presence of CFL or FL luminophores at concentrations of 100, 200, 300 mg/L for 5 days (see chapter above) were used for these analyses.
The ratio of REEs accumulated in algal biomass from these luminophores was found to differ substantially from that present in nutrient medium. They differed in the content of individual REEs (mg/g), but more importantly, in their relative proportions (%), (compare Tables 1, 2). The level of REEs accumulated from CFL luminophores was more than four times higher than those from FLs (13.01 vs 3.01 mg/g) (Table 2).
Comparing the composition of individual REEs accumulated in biomass from these luminophores, the content of yttrium was 5.6 times lower (in mg/g) from FL luminophores than from CFLs (1.98, 11.14, correspondingly) (Table 2). In contrast, lanthanum and cerium accumulated to similar concentrations (mg/g) from both luminophores (compare in Table 2) in spite of the fact that the concentration of total REEs in nutrient medium from CFL luminophores was more than twice as high as from FLs (Table 1).
Growth in the Presence of Luminophores
Cultures of G. phlegrea at the same initial concentration (about 2 × 106 cells/mL, Fig. 1a, b) were incubated mixotrophically under continuous light of incident intensity 150 µmol/m2/s1 at 39 °C in the presence of 1% glycerol for 5 days to obtain biomass for elemental analysis (see below).
The luminophore powders (FL, Fig. 2a or CFL, Fig. 2b) were added to nutrient medium at the beginning of the cultivation, at concentrations of 0, 100, 200 and 300 mg/L and growth was monitored as the number of cells per mL both in luminophore-treated (100, 200, 300) and control luminophore-free cultures (0) (Fig. 2).
Growth of all experimental variants, including the control, was exponential for two or three days as evidenced by straight lines in logarithmic scale in Fig. 2a and b. The stimulatory effects were apparent with both types of luminophores, but not equal, particularly at higher concentrations of applied REEs.
In contrast to the effect of REEs from FL, REEs from CFL had a lower stimulatory effect on growth (cell division). Practically no effect was observed in the presence of the lowest concentration (100 mg/L) (see 0 and 100 lines, Fig. 2b) whereas at higher concentrations of CFL, cell division increased but to a lesser extent than at the same concentrations of FL. An interesting inverse correlation was that in medium containing a high level of yttrium (CFL medium), cell division was stimulated less than in the presence of lower levels of yttrium (FL medium) (control: 273 106 cells/mL, CFL: 402 106 cells/mL, FL: 751 106 cells/mL), (Fig. 2c).
Differential effects of REEs from CFL or FL on cell division may be caused by qualitatively different actions of REEs on cellular structures/events in algal cells, accompanied by distinct localizations in different cellular compartments.
Yttrium, the most frequent element in both luminophores (Table 1) as well as in REEs absorbed by biomass (Table 2) might play important roles in plant physiological activities, particularly photosynthesis e.g., via binding to Rubisco or chlorophylls [38, 39]. In recent experiments, yttrium was found to stimulate the synthesis of chlorophyll and to enhance chloroplast activities (see the following subchapter). In contrast, considering lanthanides present in luminophores at low concentrations, lanthanum and cerium were found to support cellular proliferation and growth in mammals [40], plants [41, 42] as well as in algae Chlamydomonas reinhardtii, Desmodesmus quadricauda and some others including Cyanophyta [43,44,45], for review see [26, 28].
A stimulatory effect of low concentrations of lanthanum or cerium on stabilization of the cytoskeleton and division processes have repeatedly been reported [46], for review, see [47]. This may explain why, in the culture containing REEs from CFL with a high yttrium content, cells divided into fewer daughters than in cultures containing REEs from FL luminophores, with low levels of yttrium (Table 2, Fig. 2).
Variation in Pigment Content
Galdieria, as a red alga (Rhodophyta), differs substantially from frequently studied Chlorophyta, particularly in its composition of pigments, including photosynthetic ones. It contains only chlorophyll a (no chlorophyll b), a high content of carotenes, and the pigments phycoerythrin and phycocyanin (complex of phycobiliproteins, specific only for Rhodophyta and Cyanophyta). In the control culture (REE free), the color was slightly yellowish (Fig. 3, Control), which is a consequence of a relatively high content of carotenes, whose color overlaps with the green spectrum of chlorophyll a (Fig. 4, bars 0). The presence of luminophores (CFL, FL) in the nutrient medium caused an increase in both pigments in comparison with the control culture (Fig. 4). However, the increase in chlorophyll a was relatively greater than that of carotenes (Fig. 4) so the green color of cultures was due to the chlorophyll spectrum swamping the orange color of carotenes (Fig. 3). Pigment levels increased with the concentration of REEs (compare bars for values of added luminophores 100 to 300 mg/L in Fig. 4). The increase in chlorophyll a was proportionally higher than carotene (Fig. 4). Continuous growth in the presence of luminophores led to increased cell numbers (Fig. 1c) and chlorophyll content, as indicated by dark green cells (Fig. 3, bottom panel).
CFL medium, containing a high yttrium content, stimulated pigment synthesis, particularly chlorophyll a, more than the low yttrium-containing FL medium (Fig. 4). As comes from findings in fern Dicranopteris dichotoma [38], a possible explanation for this result is that the structure of yttrium-bound chlorophyll a was different from other REE-bound chlorophylls a. Where other REE-bound chlorophylls a were of a double-decker sandwich structure, yttrium-bound chlorophyll was a single layer structure that was similar to the structure of magnesium chlorophyll a. The relatively short ion radius of yttrium, compared with other REEs, might be responsible for this phenomenon, and this may play a specific role in plant photosynthesis [38].
Conclusion
Waste luminophores from energy saving bulbs (CFL) and fluorescent lamps (FL) containing REEs were analyzed both quantitatively and qualitatively. The total content of REEs differed, being two fold higher in luminophores from CFL than from FL. The most abundant element in both luminophores was yttrium, representing about 90% of total REEs. The ratios of other REEs in the luminophores varied. Thus, it is crucial in the context of any potential application, to evaluate the composition of REEs from any specific source. Cultures of G. phlegrea grew heterotrophically in the presence of 1% v/v glycerol much faster than under autotrophic conditions and to extremely high cell densities (dry matter 56 mg/L). This characteristic permits cultivation in large scale bioreactors independent of outdoor conditions.
REEs from CFL and FL accumulated in the cells during cultivation of G. phlegrea but the proportions and levels of the REEs were markedly different from the original composition of the luminophores tested.
G. phlegrea grew in growth medium containing CFL and FL luminophores up to the levels of 300 mg/L. Growth and cell division were stimulated by REEs from CFL and FL but the effect of CFL was less, possibly due to the high content of yttrium in CFL blocking cell division.
REEs from CFL and FL caused an increase in chlorophyll a and carotenes, possibly due to yttrium mimicking the structure of magnesium chlorophyll a.
These results suggest that G. phlegrea can be used for bioaccumulation of REEs from e-waste, even at low pH. This could form the basis of an environmentally-friendly technology for bioaccumulation of REEs. Mixotrophic or heterotrophic growth using cheap waste glycerol as a carbon source would be of benefit for prospective scale-up cultivation.
References
Zhu, Z., Wang, Z.G., Li, J., Li, Y., Zhang, Z.G., Zhang, P.: Distribution of rare earth elements in sewage-irrigated soil profiles in Tianjin, China. J. Rare Earths (2012). https://doi.org/10.1016/S1002-0721(12)60099-4
Halle, I., Bohme, H., Schnug, E.: Investigation on rare earth elements as growth promoting additives in diets for broilers and growing—finishing pigs. In: Proceedings 7th Conference of the ESVCN in Hanniver, vol. 101, 3rd–4 th October 2004 (2003)
Wen, B., Yuan, D.-A., Shan, X.-Q., Li, F.-L., Zhang, S.-Z.: The influence of rare earth element fertilizer application on the distribution and bioaccumulation of rare earth elements in plants under field conditions. Chem. Speciat. Bioavailab. 13, 39–48 (2001). https://doi.org/10.3184/095422901783726825
Hu, Z.H., Richter, H., Sparovek, G., Schnug, E.: Physiological and biochemical effects of rare earth elements on plants and their agricultural significance: a review. J. Plant Nutr. 27, 183–220 (2004)
Liu, X., Wang, J., Yang, J., Fan, Y., Wu, Y., Zhang, H.: Application of rare earth phosphate fertilizer in western area of China. J. Rare Earths 24, 423–426 (2006)
Emmanuel, E.S.C., Anandkumar, B., Natesan, M., Maruthamuthu, S.: Efficacy of rare earth elements on the physiological and biochemical characteristics of Zea mays L. Austral. J. Crop Sci. 4(4), 289–294 (2010)
European-Commission: Study on the review of the list of critical raw materials. Critical raw materials factsheets. Catalogue Number ET-04-15-307-ENN (2017)
Sethurajan, M., Lens, P.N.L., Horn, H.A., Figueiredo, L.H.A., van Hullebusch, E.D.: Leaching and recovery of metals. In: Rene, E.R., Lewis, A., Sahynkaya, E., Lens, P.N.L. (eds.) Sustainable heavy metal remediation. Environmental Chemistry for a Sustainable World, vol. 2, pp. 161–206. Springer, Cham (2017)
Omodara, L., Satu Pitkaaho, S., Turpeinen, E.-M., Saavalainen, P., Oravisjarvi, K., Keiski, R.L.: Recycling and substitution of light rare earth elements, cerium, lanthanum, neodymium, and praseodymium from end-of-life applications—a review. J. Clean. Prod. 236, 117573 (2019). https://doi.org/10.1016/j.jclepro.2019.07.048
Pollmann, K., Kutschke, S., Matys, S., Raff, J., Hlawacek, G., Lederer, F.L.: Bio-recycling of metals: recycling of technical products using biological applications. Biotechnol. Adv. 36(4), 1048–1062 (2018). https://doi.org/10.1016/j.biotechadv.2018.03.006
Yu, Z., Hana, H., Feng, P., Zhao, S., Zhou, T., Kakade, A., Kulshrestha, S., Majeed, S., Lia, X.: Recent advances in the recovery of metals from waste through biological processes. Bioresour. Technol. 297, 122416 (2020). https://doi.org/10.1016/j.biortech.2019.122416
Yang, D., Gao, S., Hong, J., Ye, L., Ma, X., Qi, C., Li, X.: Life cycle assessment of rare earths recovery from waste fluorescent powders—a case study in China. Waste Manag. (2019). https://doi.org/10.1016/j.wasman.2019.08.038
Barmettler, F., Castelberg, C., Fabbri, C., Brandl, H.: Microbial mobilization of rare earth elements (REE) from mineral solids—a mini review. AIMS Microbiol. 2(2), 190–204 (2016). https://doi.org/10.3934/microbiol.2016.2.190
Tanvar, H., Hukla, N., Dhawan, N.: Recycling of discarded tubular lights for recovery of rare earth values. JOM 72(2), 823–830 (2020). https://doi.org/10.1007/s11837-019-03890-1
Reed, D.W., Fujita, Y., Daubaras, D.L., Jiao, Y., Thompson, V.S.: Bioleaching of rare earth elements from waste hosphors and cracking catalysts. Hydrometallurgy 166, 34–40 (2016). https://doi.org/10.1016/j.hydromet.2016.08.006
Hopfe, S., Flemming, K., Lehmann, F., Möckel, R., Kutschke, S., Pollmann, K.: Leaching of rare earth elements from fluorescent powder using the tea fungus Kombucha. Waste Manag. 62, 211–221 (2017). https://doi.org/10.1016/j.wasman
Pourhossein, F., Mousavi, S.M.: Enhancement of copper, nickel, and gallium recovery from LED waste by adaptation of Acidithiobacillus ferrooxidans. Waste Manag. 79, 98–108 (2018). https://doi.org/10.1016/j.wasman.2018.07.010
Čížková, M., Bišová, K., Zachleder, V., Mezricky, D., Rucki, M., Vítová, M.: Utilization of rare earth elements from luminophores using green algae—laboratory scale. In: Sixth International Conference on Industrial & Hazardous Waste Management. pp. 1–7. Chania-Crete-Greece, 4–7 September 2018 (2018)
Minoda, A., Sawada, H., Suzuki, S., Miyashita, S., Inagaki, K., Yamamoto, T., Tsuzuki, M.: Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid. Appl. Microbiol. Biotechnol. 99(3), 1513–1519 (2015). https://doi.org/10.1007/s00253-014-6070-3
Jacinto, J., Henriques, B., Duarte, A.C., Vale, C., Pereira, E.: Removal and recovery of critical rare elements from contaminated waters by living Gracilaria gracilis. J. Hazard. Mater. 344, 533–538 (2018). https://doi.org/10.1016/j.jhazmat.2017.10.054
Kim, J., Dodbiba, G., Tanimra, Y., Mitsuhashi, K., Fukuda, N., Okaya, K., Matsuo, S., Fujita, T.: Leaching of rare-earth elements and their adsorption by using blue-green algae. Jpn. Inst. Met. 52(09), 1799–1806 (2011). https://doi.org/10.2320/matertrans.M2011111
Isildar, A., van Hullebusch, E.D., Lenz, M., Du Laing, G., Marra, A., Cesaro, A., Panda, S., Akcil, A., Kucuker, M.A., Kuchta, K.: Biotechnological strategies for the recovery of valuable and critical raw materials from waste electrical and electronic equipment (WEEE): a review. J. Hazard. Mater. 362, 467–481 (2019). https://doi.org/10.1016/j.jhazmat.2018.08.050
Fischer, C.B., Körsten, S., Rösken, L.M., Cappel, F., Beresko, C., Ankerhold, G., Schönleber, A., Geimer, S., Eckerf, D., Wehner, S.: Cyanobacterial promoted enrichment of rare earth elements europium, samarium and neodymium and intracellular europium particle formation†. R. Soc. Chem. Adv. 9, 32581–32593 (2019). https://doi.org/10.1039/C9RA06570A
Čížková, M., Mezricky, D., Rucki, M., Tóth, T.M., Náhlík, V., Lanta, V., Bišová, K., Zachleder, V., Vítová, M.: Bio-mining of lanthanides from red mud by green microalgae. Molecules 24(7), 1–19 (2019). https://doi.org/10.3390/molecules24071356
Goecke, F., Jerez, C.G., Zachleder, V., Figueroa, F.L., Bišová, K., Řezanka, T., Vítová, M.: Use of lanthanides to alleviate the effects of metal ion-deficiency in Desmodesmus quadricauda (Sphaeropleales, Chlorophyta). Front. Microbiol. 6(2), 1–12 (2015). https://doi.org/10.3389/fmicb.2015.00002
Goecke, F., Zachleder, V., Vítová, M.: Rare earth elements and algae: physiological effects, biorefinery and recycling. In: Prokop, A., Bajpai, R.K., Zappi, M.E. (eds.) Algal Biorefineries, Products and Refinery Design, vol. 2, pp. 339–366. Springer, Berlin (2015)
Goecke, F., Vítová, M., Lukavský, J., Nedbalová, L., Řezanka, T., Zachleder, V.: Effects of rare earth elements on growth rate, lipids, fatty acids and pigments in microalgae. Phycol. Res. 65, 226–234 (2017). https://doi.org/10.1111/pre.12180
Vítová, M., Čížková, M., Zachleder, V.: Lanthanides and algae. In: Awwad, N.S., Mubarak, A.T. (eds.) Lanthanides, pp. 87–111. Intech Open Limited, London (2019)
Čížková, M., Vítová, M., Zachleder, V.: The red microalga Galdieria as a promising organism for applications in biotechnology. In: Vítová, M. (ed.) Microalgae—From Physiology to Application, vol. 1–17. IntechOpen, London (2019)
Doemel, W.N., Brock, T.D.: The upper temperature limit of Cyanidium caldarium. Arch. Microbiol. 72, 326–332 (1970). https://doi.org/10.1007/BF00409031
Gross, W., Oesterheit, C.: Ecophysiological studies on the red alga Galdieria sulphuraria isolated from Southwest Iceland. Plant Biol. 1, 694–700 (1999). https://doi.org/10.1111/j.1438-8677.1999.tb00282.x
Graverholt, O.S., Eriksen, N.T.: Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Appl. Microbiol. Biotechnol. 77(1), 69–75 (2007). https://doi.org/10.1007/s00253-007-1150-2
Barbier, G., Ch, O., Larson, M.D., Halgren, R.G., Wilkerson, C., Garavito, M.R., Benning, C., Weber, A.P.M.: Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbo. Plant Physiol. 137, 460–474 (2005). https://doi.org/10.1104/pp.104.051169
Reeb, V., Bhattacharya, D.: The thermo-acidophilic Cyanidiophyceae (Cyanidiales). In: Seckbach, J., Chapman, D.J. (eds.) Red Algae in the Genomic Age, vol. 13, pp. 409–426. Springer, Berlin (2010)
Kucinskas, V., Jasinskas, A., Butkus, V., Jotautiene, E., Pocius, A.: Investigation of sawdust and glycerol blend biofuel briquette production and usage In: Malinovska, L., Osadcuks, V. (eds.) 14th International Scientific Conference. Engineering for Rural Development, pp. 336–341. Jelgava, Latvia (2015)
Řezanka, T., Vítová, M., Nedbalová, L., Lukavský, J.: Nutrient solution for the cultivation of photosynthetic microorganisms, process for its preparation and use (in Czech). Patent cz 306000, B6 (2016)
Wellburn, A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144(3), 307–313 (1994)
Wei, Z., Hong, F., Yin, M., Li, H., Hu, F., Zhao, G., WoonchungWong, J.: Subcellular and molecular localization of rare earth elements and structural characterization of yttrium bound chlorophyll a in naturally grown fern Dicranopteris dichotoma. Microchem. J. 80(1), 1–8 (2005). https://doi.org/10.1016/j.microc.2004.07.005
Wang, Q., Lai, Y., Yang, L., Huang, B.: Preliminary study of existing species of lanthanum in spinach leaves after being cultivated with a culture solution containing lanthanum. Anal Sci. 17, 789–791 (2001)
Naganuma, T., Traversa, E.: The effect of cerium valence states at cerium oxide nanoparticle surfaces on cell proliferation. Biomaterials 35(15), 4441–4453 (2014)
Wang, C., Shi, C., Liu, L., Wang, C., Qiao, W., Gu, Z., Wang, X.: Lanthanum element induced imbalance of mineral nutrients, HSP 70 PROduction and DNA-Protein crosslink, leading to hormetic response of cell cycle progression in root tips of Vicia faba L. seedlings. Dose Response 10(1), 96–107 (2012). https://doi.org/10.2203/dose-response.11-041.Wang
Wang, C.R., Lu, X.W., Tian, Y., Cheng, T., Hu, L.L., Chen, F.F., Jiang, C.J., Wang, X.R.: Lanthanum resulted in unbalance of nutrient elements and disturbance of cell proliferation cycles in V. faba L. seedlings. Biol. Trace Elem. Res. 143(2), 1174–1181 (2011). https://doi.org/10.1007/s12011-010-8939-z
Liu, S., Shizong, L.: Effects of La on growth and the chlorophyll contents of Chlorella in heterotrophic culture. Chin. Rare Earths 20, 38–40 (1999)
Gong, D., Li, G., Zhang, S., Chen, T.: Effect of external rare earth La3+ on growth and physiological property of Athrospira in alkaline lake of Erdos plateau. J. Chin. Soc. Rare Earths 29(4), 504–507 (2011)
Liu, Y.-F., Tang, R.-H., Zhang, Q.-X., Shi, J.-Y., Li, X.-M., Liu, Z.-Q., Zhao, W.: Stimulation of cell growth of Tetrahymena pyriformis and Chlamydomonas reinhardtii by trace elements. Biol. Trace Elem. Res. 9, 89–99 (1986)
Liu, M., Hasenstein, K.H.: La3+ uptake and its effect on the cytoskeleton in root protoplasts of Zea mays L. Planta 220(5), 658–666 (2005). https://doi.org/10.1007/s00425-004-1379-2
Horovitz, C.T.: Interactions of scandium and yttrium within cells, cellular organelles, and tissues. In: Frieden, E. (ed.) Biochemistry of Scandium and Yttrium, Part 2: Biochemistry and Applications. Biochemistry of the Elements, vol. 13B, pp. 1–38. Springer, Boston, MA (2000)
Acknowledgements
We acknowledge prof. J. D. Brooker for critical reading and language editing of the text.
Funding
The project was supported by the European fund for regional development, the program Interreg V-A Austria – Czech Republic, the Project ATCZ172 REEgain and by Institutional Research Concept No. AV0Z61388971.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Čížková, M., Mezricky, P., Mezricky, D. et al. Bioaccumulation of Rare Earth Elements from Waste Luminophores in the Red Algae, Galdieria phlegrea. Waste Biomass Valor 12, 3137–3146 (2021). https://doi.org/10.1007/s12649-020-01182-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-020-01182-3