Skip to main content

Advertisement

SpringerLink
Log in

Bioaccumulation of Rare Earth Elements from Waste Luminophores in the Red Algae, Galdieria phlegrea

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

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

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. 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

    Article  Google Scholar 

  2. 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)

  3. 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

    Article  Google Scholar 

  4. 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)

    Article  Google Scholar 

  5. 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)

    Google Scholar 

  6. 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)

    Google Scholar 

  7. 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)

  8. 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)

    Chapter  Google Scholar 

  9. 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

    Article  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

    Article  Google Scholar 

  12. 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

    Article  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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)

  19. 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

    Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. 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

    Article  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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)

    Chapter  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. 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)

    Google Scholar 

  29. 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)

    Google Scholar 

  30. 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

    Article  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    Article  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. 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)

    Chapter  Google Scholar 

  35. 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)

  36. 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)

    Google Scholar 

  37. 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)

    Article  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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)

    Article  Google Scholar 

  40. Naganuma, T., Traversa, E.: The effect of cerium valence states at cerium oxide nanoparticle surfaces on cell proliferation. Biomaterials 35(15), 4441–4453 (2014)

    Article  Google Scholar 

  41. 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

    Article  Google Scholar 

  42. 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

    Article  Google Scholar 

  43. 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)

    Google Scholar 

  44. 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)

    Google Scholar 

  45. 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)

    Article  Google Scholar 

  46. 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

    Article  Google Scholar 

  47. 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)

    Chapter  Google Scholar 

Download references

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

  1. Laboratory of Cell Cycles of Algae, Centre Algatech, Institute of Microbiology of the Czech Academy of Sciences, Novohradská 237, 379 81, Třeboň, Czech Republic

    Mária Čížková, Vilém Zachleder & Milada Vítová

  2. Medical and Pharmaceutical Biotechnology, IMC University of Applied Sciences, Piaristengasse 1, 3500, Krems, Austria

    Pauline Mezricky & Dana Mezricky

  3. Laboratory of Predictive Toxicology, National Institute of Public Health, Šrobárova 48, 100 42, Prague, Czech Republic

    Marian Rucki

Authors
  1. Mária Čížková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pauline Mezricky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dana Mezricky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marian Rucki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vilém Zachleder
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Milada Vítová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Milada Vítová.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-020-01182-3

Keywords

Search

Navigation