In recent decades, a shift has been seen in the use of light-emitting diodes over incandescent lights and compact fluorescent lamps (CFL), which eventually led to an increase in wastes of electrical equipment (WEE), especially fluorescent lamps (FLs) and CFL light bulbs. These widely used CFL lights, and their wastes are good sources of rare earth elements (REEs), which are desirable in almost every modern technology. Increased demand for REEs and their irregular supply have exerted pressure on us to seek alternative sources that may fulfill this demand in an eco-friendly manner. Bio-removal of wastes containing REEs, and their recycling may be a solution to this problem and could balance environmental and economic benefits. To address this problem, the current study focuses on the use of the extremophilic red alga, Galdieria sulphuraria, for bioaccumulation/removal of REEs from hazardous industrial wastes of CFL bulbs and the physiological response of a synchronized culture of G. sulphuraria. A CFL acid extract significantly affected growth, photosynthetic pigments, quantum yield, and cell cycle progression of this alga. A synchronous culture was able to efficiently accumulate REEs from a CFL acid extract and efficiency was increased by including two phytohormones, i.e., 6-Benzylaminopurine (BAP - Cytokinin family) and 1-Naphthaleneacetic acid (NAA - Auxin family).

Centre for Phycology Institute of Botany Czech Academy of Sciences Třeboň Czechia

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Institute of Aquaculture and Protection of Waters University of South Bohemia České Budějovice Czechia

Institute of Medical and Pharmaceutical Biotechnology IMC FH Krems Krems Austria

Laboratory of Cell Cycles of Algae Centre Algatech Institute of Microbiology Czech Academy of Sciences Třeboň Czechia

Laboratory of Predictive Toxicology National Institute of Public Health Prague Czechia

Zobrazit více v PubMed

Abiusi F., Fernández P. M., Cansiani S., Janssen M., Wijffels R. H., Barbosa M. (2022). Mixotrophic cultivation of Galdieria sulphuraria for C-phycocyanin and protein production. Algal Res. 61:102603. doi: 10.1016/j.algal.2021.102603 DOI

Ashraf N., Vítová M., Cloetens P., Mijovilovich A., Bokhari S. N. H., Küpper H. (2021). Effect of nanomolar concentrations of lanthanum on Desmodesmus quadricauda cultivated under environmentally relevant conditions. Aquat. Toxicol. 235:105818. doi: 10.1016/j.aquatox.2021.105818, PMID: PubMed DOI

Balaram V. (2019). Rare earth elements: a review of applications, occurrence, exploration, analysis, recycling, and environmental impact. Geosci. Front. 10, 1285–1303. doi: 10.1016/j.gsf.2018.12.005 DOI

Baldé C. P., Forti V., Gray V., Kuehr R., Stegmann P. (2017). The Global e-Waste Monitor 2017: Quantities, Flows and Resources. Bonn/Geneva/Vienna: United Nations University, International Telecommunication Union, and International Solid Waste Association.

Bennett A., Bogorad L. (1973). Complementary chromatic adaptation in a filamentous blue-green alga. J. Cell Biol. 58, 419–435. doi: 10.1083/jcb.58.2.419, PMID: PubMed DOI PMC

Bottone C., Camerlingo R., Miceli R., Salbitani G., Sessa G., Pirozzi G., et al. . (2019). Antioxidant and anti-proliferative properties of extracts from heterotrophic cultures of Galdieria sulphuraria. Nat. Prod. Res. 33, 1659–1663. doi: 10.1080/14786419.2018.1425853, PMID: PubMed DOI

Brányiková I., Maršálková B., Doucha J., Brányik T., Bišová K., Zachleder V., et al. . (2011). Microalgae—novel highly efficient starch producers. Biotechnol. Bioeng. 108, 766–776. doi: 10.1002/bit.23016, PMID: PubMed DOI

Carfagna S., Landi V., Coraggio F., Salbitani G., Vona V., Pinto G., et al. . (2018). Different characteristics of C-phycocyanin (C-PC) in two strains of the extremophilic Galdieria phlegrea. Algal Res. 31, 406–412. doi: 10.1016/j.algal.2018.02.030 DOI

Carfagna S., Napolitano G., Barone D., Pinto G., Pollio A., Venditti P. (2015). Dietary supplementation with the microalga Galdieria sulphuraria (Rhodophyta) reduces prolonged exercise-induced oxidative stress in rat tissues. Oxidative Med. Cell. Longev. 2015, 1–11. doi: 10.1155/2015/732090, PMID: PubMed DOI PMC

Chakhmouradian A. R., Wall F. (2012). Rare earth elements: minerals, mines, magnets (and more). Elements 8, 333–340. doi: 10.2113/gselements.8.5.333 DOI

Cheisson T., Schelter E. J. (2019). Rare earth elements: Mendeleev’s bane, modern marvels. Science 363, 489–493. doi: 10.1126/science.aau7628, PMID: PubMed DOI

Cheng J., Qiu H., Chang Z., Jiang Z., Yin W. (2016). The effect of cadmium on the growth and antioxidant response for freshwater algae Chlorella vulgaris. Springer Plus 5:1290. doi: 10.1186/s40064-016-2963-1, PMID: PubMed DOI PMC

Čížková M., Mezricky P., Mezricky D., Rucki M., Zachleder V., Vítová M. (2021). Bioaccumulation of rare earth elements from waste luminophores in the red algae, Galdieria phlegrea. Waste and Biomass Valorization 12, 3137–3146. doi: 10.1007/s12649-020-01182-3 DOI

Čížková M., Vítová M., Zachleder V. (2019). The red microalga Galdieria as a promising organism for applications in biotechnology. Microalgae Physiol. Appl. 1:17. doi: 10.5772/intechopen.89810 DOI

Dubey K., Dubey K. P. (2011). A study of the effect of red mud amendments on the growth of cyanobacterial species. Biorem. J. 15, 133–139. doi: 10.1080/10889868.2011.598483 DOI

Edmundson S. J., Huesemann M. H. (2015). The dark side of algae cultivation: characterizing night biomass loss in three photosynthetic algae, Chlorella sorokiniana, Nannochloropsis Salina and Picochlorum sp. Algal Res. 12, 470–476. doi: 10.1016/j.algal.2015.10.012 DOI

Ferraro G., Imbimbo P., Marseglia A., Lucignano R., Monti D. M., Merlino A. (2020). X-ray structure of C-phycocyanin from Galdieria phlegrea: determinants of thermostability and comparison with a C-phycocyanin in the entire phycobilisome. Biochim. Biophys. Acta Bioenerg. 1861:148236. doi: 10.1016/j.bbabio.2020.148236, PMID: PubMed DOI

Fu H.-Y., Liu S.-L., Chiang Y.-R. (2020). Biosynthesis of ascorbic acid as a glucose-induced photoprotective process in the extremophilic red alga Galdieria partita. Front. Microbiol. 10:3005. doi: 10.3389/fmicb.2019.03005, PMID: PubMed DOI PMC

Gauthier M. R., Senhorinho G. N. A., Scott J. A. (2020). Microalgae under environmental stress as a source of antioxidants. Algal Res. 52:102104. doi: 10.1016/j.algal.2020.102104 DOI

Goecke F., Vítová M., Lukavský J., Nedbalová L., Řezanka T., Zachleder V. (2017). Effects of rare earth elements on growth rate, lipids, fatty acids and pigments in microalgae. Phycol. Res. 65, 226–234. doi: 10.1111/pre.12180 DOI

González V., Vignati D. A., Pons M.-N., Montarges-Pelletier E., Bojic C., Giamberini L. (2015). Lanthanide ecotoxicity: first attempt to measure environmental risk for aquatic organisms. Environ. Pollut. 199, 139–147. doi: 10.1016/j.envpol.2015.01.020, PMID: PubMed DOI

Gross W., Kuever J., Tischendorf G., Bouchaala N., Büsch W. (1998). Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur. J. Phycol. 33, 25–31. doi: 10.1080/09670269810001736503 DOI

Guterman H., Ben-Yaakov S., Vonshak A. (1989). Automatic on-line growth estimation method for outdoor algal biomass production. Biotechnol. Bioeng. 34, 143–152. doi: 10.1002/bit.260340202, PMID: PubMed DOI

Gwenzi W., Mangori L., Danha C., Chaukura N., Dunjana N., Sanganyado E. (2018). Sources, behaviour, and environmental and human health risks of high-technology rare earth elements as emerging contaminants. Sci. Total Environ. 636, 299–313. doi: 10.1016/j.scitotenv.2018.04.235, PMID: PubMed DOI

Hu Q., Kurano N., Kawachi M., Iwasaki I., Miyachi S. (1998). Ultrahigh-cell-density culture of a marine green alga Chlorococcum littorale in a flat-plate photobioreactor. Appl. Microbiol. Biotechnol. 49, 655–662. doi: 10.1007/s002530051228 DOI

Hu Z., Richter H., Sparovek G., Schnug E. (2004). Physiological and biochemical effects of rare earth elements on plants and their agricultural significance: a review. J. Plant Nutr. 27, 183–220. doi: 10.1081/PLN-120027555 DOI

Iovinella M., Carbone D. A., Cioppa D., Davis S. J., Innangi M., Esposito S., et al. . (2020). Prevalent pH controls the capacity of Galdieria maxima to use ammonia and nitrate as a nitrogen source. Plan. Theory 9:232. doi: 10.3390/plants9020232, PMID: PubMed DOI PMC

Jalali J., Lebeau T. (2021). The role of microorganisms in mobilization and phytoextraction of rare earth elements: a review. Front. Environ. Sci. 9:688430. doi: 10.3389/fenvs.2021.688430 DOI

Johnson E. M., Kumar K., Das D. (2014). Physicochemical parameters optimization, and purification of phycobiliproteins from the isolated Nostoc sp. Bioresour. Technol. 166, 541–547. doi: 10.1016/j.biortech.2014.05.097, PMID: PubMed DOI

Jong L. W., Fujiwara T., Hirooka S., Miyagishima S.-Y. (2021). Cell size for commitment to cell division and number of successive cell divisions in cyanidialean red algae. Protoplasma 258, 1103–1118. doi: 10.1007/s00709-021-01628-y, PMID: PubMed DOI

Kselíková V., Husarčíková K., Zachleder V., Bišová K. (2022). Cultivation of the microalgae Chlamydomonas reinhardtii and Desmodesmus quadricauda in highly deuterated media: balancing the light intensity. Front. Bioeng. Biotechnol. 10:960862. doi: 10.3389/fbioe.2022.960862, PMID: PubMed DOI PMC

Lima A. T., Ottosen L. (2021). Recovering rare earth elements from contaminated soils: critical overview of current remediation technologies. Chemosphere 265:129163. doi: 10.1016/j.chemosphere.2020.129163, PMID: PubMed DOI

Liu A., Shizong L. (1999). Effects of La on growth and the chlorophyll contents of Chlorella in heterotrophic culture. Chin. Rare Earths 20, 38–40.

Machado M. D., Soares E. V. (2014). Modification of cell volume and proliferative capacity of Pseudokirchneriella subcapitata cells exposed to metal stress. Aquat. Toxicol. 147, 1–6. doi: 10.1016/j.aquatox.2013.11.017, PMID: PubMed DOI

Martinez-Garcia M., Kormpa A., Van Der Maarel M. J. (2017). The glycogen of Galdieria sulphuraria as alternative to starch for the production of slowly digestible and resistant glucose polymers. Carbohydr. Polym. 169, 75–82. doi: 10.1016/j.carbpol.2017.04.004, PMID: PubMed DOI

McCready R., Guggolz J., Silviera V., Owens H. (1950). Determination of starch and amylose in vegetables. Anal. Chem. 22, 1156–1158. doi: 10.1021/ac60045a016 DOI

Minoda A., Sawada H., Suzuki S., Miyashita S.-I., Inagaki K., Yamamoto T., et al. . (2015). Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid. Appl. Microbiol. Biotechnol. 99, 1513–1519. doi: 10.1007/s00253-014-6070-3, PMID: PubMed DOI

Náhlík V., Čížková M., Singh A., Mezricky D., Rucki M., Andresen E., et al. . (2022). Growth of the red alga Galdieria sulphuraria in red mud-containing medium and accumulation of rare earth elements. Waste Biomass Valorization. doi: 10.1007/s12649-022-02021-3 DOI

Náhlík V., Zachleder V., Čížková M., Bišová K., Singh A., Mezricky D., et al. . (2021). Growth under different trophic regimes and synchronization of the red microalga Galdieria sulphuraria. Biomol. Ther. 11:939. doi: 10.3390/biom11070939, PMID: PubMed DOI PMC

Oesterhelt C., Schmälzlin E., Schmitt J. M., Lokstein H. (2007). Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria. Plant J. 51, 500–511. doi: 10.1111/j.1365-313X.2007.03159.x, PMID: PubMed DOI

Pagano G., Thomas P. J., Di Nunzio A., Trifuoggi M. (2019). Human exposures to rare earth elements: present knowledge and research prospects. Environ. Res. 171, 493–500. doi: 10.1016/j.envres.2019.02.004, PMID: PubMed DOI

Pinto J., Costa M., Henriques B., Soares J., Dias M., Viana T., et al. . (2021). Competition among rare earth elements on sorption onto six seaweeds. J. Rare Earths 39, 734–741. doi: 10.1016/j.jre.2020.09.025 DOI

Pinto J., Henriques B., Soares J., Costa M., Dias M., Fabre E., et al. . (2020). A green method based on living macroalgae for the removal of rare-earth elements from contaminated waters. J. Environ. Manag. 263:110376. doi: 10.1016/j.jenvman.2020.110376, PMID: PubMed DOI

Pinto E., Sigaud-Kutner T. C. S., Leitao M. A. S., Okamoto O. K., Morse D., Colepicolo P. (2003). Heavy metal-induced oxidative stress in algae. J. Phycol. 39, 1008–1018. doi: 10.1111/j.0022-3646.2003.02-193.x DOI

Piotrowska-Niczyporuk A., Bajguz A., Zambrzycka E., Godlewska-Żyłkiewicz B. (2012). Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol. Biochem. 52, 52–65. doi: 10.1016/j.plaphy.2011.11.009, PMID: PubMed DOI

Piotrowska-Niczyporuk A., Bajguz A., Zambrzycka-Szelewa E., Bralska M. (2018). Exogenously applied auxins and cytokinins ameliorate lead toxicity by inducing antioxidant defence system in green alga Acutodesmus obliquus. Plant Physiol. Biochem. 132, 535–546. doi: 10.1016/j.plaphy.2018.09.038, PMID: PubMed DOI

Potijun S., Yaisamlee C., Sirikhachornkit A. (2021). Pigment production under cold stress in the green microalga Chlamydomonas reinhardtii. Agriculture 11:564. doi: 10.3390/agriculture11060564 DOI

Qu Y., Lian B. (2013). Bioleaching of rare earth and radioactive elements from red mud using Penicillium tricolor RM-10. Bioresour. Technol. 136, 16–23. doi: 10.1016/j.biortech.2013.03.070, PMID: PubMed DOI

Reeb V., Bhattacharya D. (2010). “The thermo-acidophilic cyanidiophyceae (Cyanidiales)” in Red Algae in the Genomic Age (Dordrecht: Springer; ), 409–426.

Schreiber U., Schliwa U., Bilger W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10, 51–62. doi: 10.1007/BF00024185, PMID: PubMed DOI

Shi T.-Q., Wang L.-R., Zhang Z.-X., Sun X.-M., Huang H. (2020). Stresses as first-line tools for enhancing lipid and carotenoid production in microalgae. Front. Bioeng. Biotechnol. 8:610. doi: 10.3389/fbioe.2020.00610, PMID: PubMed DOI PMC

Sun X., Zhong Y., Huang Z., Yang Y. (2014). Selenium accumulation in unicellular green alga Chlorella vulgaris and its effects on antioxidant enzymes and content of photosynthetic pigments. PLoS One 9:e112270. doi: 10.1371/journal.pone.0112270, PMID: PubMed DOI PMC

Torzillo G., Sacchi A., Materassi R., Richmond A. (1991). Effect of temperature on yield and night biomass loss in Spirulina platensis grown outdoors in tubular photobioreactors. J. Appl. Phycol. 3, 103–109. doi: 10.1007/BF00003691 DOI

Vítová M., Bišová K., Kawano S., Zachleder V. (2015). Accumulation of energy reserves in algae: from cell cycles to biotechnological applications. Biotechnol. Adv. 33, 1204–1218. doi: 10.1016/j.biotechadv.2015.04.012, PMID: PubMed DOI

Wan M., Zhao H., Guo J., Yan L., Zhang D., Bai W., et al. . (2021). Comparison of C-phycocyanin from extremophilic Galdieria sulphuraria and Spirulina platensis on stability and antioxidant capacity. Algal Res. 58:102391. doi: 10.1016/j.algal.2021.102391 DOI

Weber A. P., Horst R. J., Barbier G. G., Oesterhelt C. (2007). Metabolism and metabolomics of eukaryotes living under extreme conditions. Int. Rev. Cytol. 256, 1–34. doi: 10.1016/S0074-7696(07)56001-8, PMID: PubMed DOI

Wellburn A. R. (1994). 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, 307–313. doi: 10.1016/S0176-1617(11)81192-2 DOI

Yang G., Wilkinson K. J. (2018). Biouptake of a rare earth metal (Nd) by Chlamydomonas reinhardtii – bioavailability of small organic complexes and role of hardness ions. Environ. Pollut. 243, 263–269. doi: 10.1016/j.envpol.2018.08.066, PMID: PubMed DOI

Yoon H. S., Ciniglia C., Wu M., Comeron J. M., Pinto G., Pollio A., et al. . (2006). Establishment of endolithic populations of extremophilic Cyanidiales (Rhodophyta). BMC Evol. Biol. 6:78. doi: 10.1186/1471-2148-6-78, PMID: PubMed DOI PMC

Yoshimura E., Nagasaka S., Sato Y., Satake K., Mori S. (1999). Extraordinary high aluminium tolerance of the acidophilic thermophilic alga, Cyanidium caldarium. Soil Sci. Plant Nutr. 45, 721–724. doi: 10.1080/00380768.1999.10415835 DOI

Microbial recovery of rare earth elements from various waste sources: a mini review with emphasis on microalgae