microalgae; metal stress; industrial products; growth rate; metal resistance
Abstract :
[en] Microalgae are a source of numerous compounds that can be used in many branches of industry. Synthesis of such compounds in microalgal cells can be amplified under stress conditions. Exposure to various metals can be one of methods applied to induce cell stress and synthesis of target products in microalgae cultures. In this review, the potential of producing diverse biocompounds (pigments, lipids, exopolymers, peptides, phytohormones, arsenoorganics, nanoparticles) from microalgae cultures upon exposure to various metals, is evaluated. Additionally, different methods to alter microalgae response towards metals and metal stress are described. Finally, possibilities to sustain high growth rates and productivity of microalgal cultures in the presence of metals are discussed.
Disciplines :
Biotechnology
Author, co-author :
Miazek, Krystian ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie biologique industrielle
Iwanek, Waldemar
Remacle, Claire ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Richel, Aurore ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie biologique industrielle
Goffin, Dorothée ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie biologique industrielle
Language :
English
Title :
Effect of Metals, Metalloids and Metallic Nanoparticles on Microalgae Growth and Industrial Product Biosynthesis: A Review
Publication date :
09 October 2015
Journal title :
International Journal of Molecular Sciences
ISSN :
1661-6596
eISSN :
1422-0067
Publisher :
Molecular Diversity Preservation International (MDPI), Basel, Switzerland
Leliaert, F.; Smith, D.R.; Moreau, H.; Herron, M.D.; Verbruggen, H.; Delwiche, C.F.; de Clerck, O. Phylogeny and molecular evolution of the green algae. CRC Crit. Rev. Plant Sci. 2012, 31, 1–46.
Scott, J.L.; Baca, B.; Ott, F.D.; West, J.A. Light and electron microscopic observations on Erythrolobus coxiae gen.et sp. nov. (Porphyrideophyceae, Rhodophyta) from Texas U.S.A. Algae 2006, 21, 407–416.
Mann, D.G. The species concept in diatoms. Phycologia 1999, 38, 437–495.
Hackett, J.D.; Anderson, D.M.; Erdner, D.L.; Bhattacharya, D. Dinoflagellates: A remarkable evolutionary experiment. Am. J. Bot. 2004, 91, 1523–1534.
Komarek, J. Cyanobacterial taxonomy: Current problems and prospects for the integration of traditional and molecular approaches. Algae 2006, 21, 349–375.
Lowrey, J.; Brooks, M.S.; McGinn, P.J. Heterotrophic and mixotrophic cultivation of microalgae for biodiesel production in agricultural wastewaters and associated challenges—A critical review. J. Appl. Phycol. 2015, 27, 1485–1498.
Shukla, S.P.; Kviderova, J.; Triska, J.; Elster, J. Chlorella mirabilis as a potential species for biomass production in low-temperature environment. Front. Microbiol. 2013, 4, 97.
Bleeke, F.; Rwehumbiza, V.M.; Winckelmann, D.; Klöck, G. Isolation and characterization of new temperature tolerant microalgal strains for biomass production. Energies 2014, 7, 7847–7856.
Varshney, P.; Mikulic, P.; Vonshak, A.; Beardall, J.; Wangikar, P.P. Extremophilic micro-algae and their potential contribution in biotechnology. Bioresour. Technol. 2015, 184, 363–372.
Markou, G.; Nerantzis, E. Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions. Biotechnol. Adv. 2013, 31, 1532–1542.
Tangahu, B.V.; Abdullah, S.R.S.; Basri, H.; Idris, M.; Anuar, N.; Mukhlisin, M. A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int. J. Chem. Eng. 2011, doi:10.1155/2011/939161.
Monteiro, C.M.; Castro, P.M.L.; Malcata, F.X. Metal uptake by microalgae: Underlying mechanisms and practical applications. Biotechnol. Prog. 2012, 28, 299–311.
Von Moos, N.; Slaveykova, V.I. Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae—State of the art and knowledge gaps. Nanotoxicology 2013, 1–26.
Gonzalez, V.; Vignati, D.A.L.; Leyval, C.; Giamberini, L. Environmental fate and ecotoxicity of lanthanides: Are they a uniform group beyond chemistry? Environ. Int. 2014, 71, 148–157.
Aral, H.; Vecchio-Sadus, A. Toxicity of lithium to humans and the environment—A literature review. Ecotoxicol. Environ. Saf. 2008, 70, 349–356.
Andersen, R.A. Algal Culturing Techniques; Elsevier Academic Press: San Diego, CA, USA, 2005; ISBN 978-0-12-088426-1.
Moroney, J.V.; Bartlett, S.G.; Samuelsson, G. Carbonic anhydrases in plants and algae. Plant Cell Environ. 2001, 24, 141–153.
Sunda, W.G. Feedback interactions between trace metal nutrients and phytoplankton in the ocean. Front. Microbiol. 2012, doi:10.3389/fmicb.2012.00204.
Vega, J.M.; Herrera, J.; Aparicio, P.J.; Paneque, A.; Losada, M. Role of molybdenum in nitrate reduction by Chlorella. Plant Physiol. 1971, 48, 294–299.
Nishikawa, K.; Yamakoshi, Y.; Uemura, I.; Tominaga, N. Ultrastructural changes in Chlamydomonas acidophila (Chlorophyta) induced by heavy metals and polyphosphate metabolism. FEMS Microbiol. Ecol. 2003, 44, 253–259.
Carfagna, S.; Lanza, N.; Salbitani, G.; Basile, A.; Sorbo, S.; Vona, V. Physiological and morphological responses of lead and cadmium exposed Chlorella sorokiniana 211-8K (Chlorophyceae). Springerplus 2013, 2, 147.
Aoki, M.; Matsumoto, H.; Takahashi, T.; Sato, K.; Kumata, H.; Fujiwara, K. Thallium Induces Morphological Changes in the Photosynthetic Apparatus of Synechocystis sp. PCC6803; In Photosynthesis: Research for Food, Fuel and Future—15th International Conference on Photosynthesis; Zhejiang University Press: Hangzhou, China, 2013; pp. 586–589.
Andosch, A.; Hoftberger, M.; Lutz, C.; Lutz-Meindl, U. Subcellular sequestration and impact of heavy metals on the ultrastructure and physiology of the multicellular freshwater alga Desmidium swartzii. Int. J. Mol. Sci. 2015, 16, 10389–10410.
Sacan, M.T.; Oztay, F.; Bolkent, S. Exposure of Dunaliella tertiolecta to lead and aluminum: Toxicity and effects on ultrastructure. Biol. Trace Elem. Res. 2007, 120, 264–272.
Yingjun, W.; Jia, L.; Yun, L.; Hangbiao, J.; Shihuai, D.; Yunmin, Z. Effects of cerium on growth and physiological characteristics of Anabaena flosaquae. J. Rare Earths 2012, 30, 1287–1292.
Nordi, C.S.F.; Cavagliere, T.G.W.F.; Vieira, A.A.H.; Nascimento, O.R. Efeito caotrópico do íon lítio na permeabilidade da cápsula polissacarídica da microalga Ankistrodesmus gracilis (Reinsch) Korsikov (Chlorophyceae). Acta Bot. Bras. 2006, 20, 449–454.
Karlander, E.P.; Krauss, R.W. Absorption and toxicity of beryllium and lithium in Chlorella vannielii Shihira and Krauss. Chesap. Sci. 1972, 13, 245–253.
Mota, R.; Pereira, S.B.; Meazzini, M.; Fernandes, R.; Santos, A.; Evans, C.A.; de Philippis, R.; Wright, P.C.; Tamagnini, P. Effects of heavy metals on Cyanothece sp. CCY 0110 growth, extracellular polymeric substances (EPS) production, ultrastructure and protein profiles. J. Proteom. 2015, 120, 75–94.
Basharina, T.N.; Danilovtseva, E.N.; Zelinskiy, S.N.; Klimenkov, I.V.; Likhoshway, Y.V.; Annenkov, V.V. The effect of titanium, zirconium and tin on the growth of diatom Synedra acus and morphology of its silica valves. Silicon 2012, 4, 239–249.
El-Sheekh, M.M.; el-Naggar, A.H.; Osman, M.E.H.; el-Mazaly, E. Effect of cobalt on growth, pigments and the photosynthetic electron transport in Monoraphidium minutum and Nitzchia perminuta. Braz. J. Plant Physiol. 2003, 15, 159–166.
Ferrari, S.G.; Silva, P.G.; Gonzalez, D.M.; Navoni, J.A.; Silva, H.J. Arsenic tolerance of cyanobacterial strains with potential use in biotechnology. Rev. Argent. Microbiol. 2013, 45, 174–179.
Karadjova, I.B.; Slaveykova, V.I.; Tsalev, D.L. The biouptake and toxicity of arsenic species on the green microalga Chlorella salina in seawater. Aquat. Toxicol. 2008, 87, 264–271.
Knauer, K.; Hemond, H. Accumulation and reduction of arsenate by the freshwater green alga Chlorella sp. (Chlorophyta). J. Phycol. 2000, 36, 506–509.
Meisch, H.U.; Bielig, H.J. Effect of vanadium on growth, chlorophyll formation and iron metabolism in unicellular green algae. Arch. Microbiol. 1975, 105, 77–82.
Meisch, H.U.; Benzschawel, H.; Bielig, H.J. The role of vanadium in green plants. Arch. Microbiol. 1977, 114, 67–70.
Tran, N.P.; Park, J.K.; Kim, Z.H.; Lee, C.G. Influence of sodium orthovanadate on the production of astaxanthin from green algae Haematococcus lacustris. Biotechnol. Bioprocess Eng. 2009, 14, 322–329.
Fargasova, A.; Bumbalova, A.; Havranek, E. Ecotoxicological effects and uptake of metals (Cu+, Cu2+, Mn2+, Mo6+, Ni2+, V5+) in freshwater alga Scenedesmus quadricauda. Chemosphere 1999, 38, 1165–1173.
Goecke, F.; Jerez, C.G.; Zachleder, V.; Figueroa, F.L.; Rezanka, T.; Bisova, K.; Vitova, M. Use of lanthanides to alleviate the effects of metal ion-deficiency in Desmodesmus quadricauda (Sphaeropleales, Chlorophyta). Front. Microbiol. 2015, 6, 2.
Jin, X.; Chu, Z.; Yan, F.; Zeng, Q. Effects of lanthanum(III) and EDTA on the growth and competition of Microcystis aeruginosa and Scenedesmus quadricauda. Limnologica 2009, 39, 86–93.
Tai, P.; Zhao, Q.; Su, D.; Li, P.; Stagnitti, F. Biological toxicity of lanthanide elements on algae. Chemosphere 2010, 80, 1031–1035.
Lee, J.G.; Roberts, S.B.; Morel, F.M.M. Cadmium: A nutrient for the marine diatom Thalassiosira weissflogii. Limnol. Oceanogr. 1995, 40, 1056–1063.
Alterio, V.; Langella, E.; de Simone, G.; Monti, S.M. Cadmium-containing carbonic anhydrase CDCA1 in marine diatom Thalassiosira weissflogii. Mar. Drugs 2015, 13, 1688–1697.
Rees, T.A.V., Bekheet, I.A. The role of nickel in urea assimilation by algae. Planta 1982, 156, 385–387.
Oliveira, L.; Antia, N.J. Evidence of nickel ion requirement for autotrophic growth of a marine diatom with urea serving as nitrogen source. Br. Phycol. J. 1984, 19, 125–134.
Egleston, E.S.; Morel, F.M.M. Nickel limitation and zinc toxicity in a urea-grown diatom. Limnol. Oceanogr. 2008, 53, 2462–2471.
Xia, B.; Chen, B.; Sun, X.; Qu, K.; Ma, F.; Du, M. Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: Growth inhibition, oxidative stress and internalization. Sci. Total Environ. 2015, 508, 525–533.
Suman, T.Y.; Rajasree, S.R.R.; Kirubagaran, R. Evaluation of zinc oxide nanoparticles toxicity on marine algae Chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicol. Environ. Saf. 2015, 113, 23–30.
Castro-Bugallo, A.; Gonzalez-Fernandez, A.; Guisande, C.; Barreiro, A. Comparative responses to metal oxide nanoparticles in marine phytoplankton. Arch. Environ. Contam. Toxicol. 2014, 67, 483–493.
Lee, W.M.; An, Y.J. Effects of zinc oxide and titanium dioxide nanoparticles on green algae under visible, UVA, and UVB irradiations: No evidence of enhanced algal toxicity under UV pre-irradiation. Chemosphere 2013, 91, 536–544.
Aravantinou, A.F.; Tsarpali, V.; Dailianis, S.; Manariotis, I.D. Effect of cultivation media on the toxicity of ZnO nanoparticles to freshwater and marine microalgae. Ecotoxicol. Environ. Saf. 2015, 114, 109–116.
Sadiq, I.M.; Pakrashi, S.; Chandrasekaran, N.; Mukherjee, A. Studies on toxicity of aluminum oxide (Al2O3) nanoparticles to microalgae species: Scenedesmus sp. and Chlorella sp. J. Nanopart. Res. 2011, 13, 3287–3299.
Manier, N.; Bado-Nilles, A.; Delalain, P.; Aguerre-Chariol, O.; Pandard, P. Ecotoxicity of non-aged and aged CeO2 nanomaterials towards freshwater microalgae. Environ. Pollut. 2013, 180, 63–70.
Manzo, S.; Miglietta, M.L.; Rametta, G.; Buono, S.; Francia, G.D. Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta. Sci. Total Environ. 2013, 445–446, 371–376.
Padrova, K.; Lukavsky, J.; Nedbalova, L.; Cejkova, A.; Cajthaml, T.; Sigler, K.; Vitova, M.; Rezanka, T. Trace concentrations of iron nanoparticles cause overproduction of biomass and lipids during cultivation of cyanobacteria and microalgae. J. Appl. Phycol. 2015, 27, 1443–1451.
Capolino, E.; Tredici, M.; Pepi, M.; Baldi, F. Tolerance to mercury chloride in Scenedesmus strains. BioMetals 1997, 10, 85–94.
Chen, C.Y.; Lin, K.C. Optimization and performance evaluation of the continuous algal toxicity test. Environ. Toxicol. Chem. 1997, 16, 1337–1344.
Gissi, F.; Adams, M.S.; King, C.K.; Jolley, D.F. Robust bioassay to assess the toxicity of metals to the Antarctic marine microalga Phaeocyctis antarctica. Environ. Toxicol. Chem. 2015, doi:10.1002/etc.2949.
D’ors, A.; Pereira, M.; Bartolome, M.C.; Lopez-Rodas, V.; Costas, E.; Sanchez-Fortun, S. Toxic effects and specific chromium acquired resistance in selected strains of Dyctiosphaerium chlorelloides. Chemosphere 2010, 81, 282–287.
Millach, L.; Sole, A.; Esteve, I. Role of Geitlerinema sp. DE2011 and Scenedesmus sp. DE2009 as bioindicators and immobilizers of chromium in a contaminated natural environment. Biomed. Res. Int. 2015, doi:10.1155/2015/519769.
Hörcsik, Z.; Oláh, V.; Balogh, A.; Mészáros, I.; Simon, L.; Lakatos, G. Effect of Chromium(VI) on growth, element and photosynthetic pigment composition of Chlorella pyrenoidosa. Acta Biol. Szeged. 2006, 50, 19–23.
Ouyang, H.L.; Kong, X.Z.; He, W.; Qin, N.; He, Q.S.; Wang, Y.; Wang, R.; Xu, F.L. Effects of five heavy metals at sub-lethal concentrations on the growth and photosynthesis of Chlorella vulgaris. Chin. Sci. Bull. 2012, 57, 3363–3370.
Levy, J.L.; Stauber, J.L.; Adams, M.S.; Maher, W.A.; Kirby, J.K.; Jolley, D.F. Toxicity, biotransformation, and mode of action of arsenic in two freshwater microalgae (Chlorella sp. and Monoraphidium arcuatum). Environ. Toxicol. Chem. 2005, 24, 2630–2639.
Rahman, M.A.; Hogan, B.; Duncan, E.; Doyle, C.; Krassoi, R.; Rahman, M.M.; Naidu, R.; Lim, R.P.; Maher, W.; Hassler, C. Toxicity of arsenic species to three freshwater organisms and biotransformation of inorganic arsenic by freshwater phytoplankton (Chlorella sp. CE-35). Ecotoxicol. Environ. Saf. 2014, 106, 126–135.
Huang, W.J.; Wu, C.C.; Chang, W.C. Bioaccumulation and toxicity of arsenic in cyanobacteria cultures separated from a eutrophic reservoir. Environ. Monit. Assess. 2014, 186, 805–814.
Trenfield, M.A.; van Dam, J.W.; Harford, A.J.; Parry, D.; Streten, C.; Gibb, K.; van Dam, R.A. Aluminium, gallium and molybdenum toxicity to the tropical marine microalga Isochrysis galbana. Environ. Toxicol. Chem. 2015, doi:10.1002/etc.2996.
Bascik-Remisiewicz, A.; Tukaj, Z. Toxicity of inorganic cadmium salts to the microalga Scenedesmus armatus (Chiorophyta) with respect to medium composition, pH and CO2 concentration. Acta Physiol. Plant. 2002, 24, 59–65.
Nohomovich, B.; Nguyen, B.T.; Quintanilla, M.; Lee, L.H.; Murray, S.R.; Chu, T.C. Physiological effects of nickel chloride on the freshwater cyanobacterium Synechococcus sp. IU 625. Adv. Biosci. Biotechnol. 2013, 4, 10–14.
Hassler, C.S.; Chafin, R.D.; Klinger, M.B.; Twiss, M.R. Application of the biotic ligand model to explain potassium interaction with thallium uptake and toxicity to plankton. Environ. Toxicol. Chem. 2007, 26, 1139–1145.
Aoki, M.; Suematsu, H.; Kumata, H.; Fujiwara, K. Physiological and photosynthetic toxicity of thallium in Synechocystis sp. PCC6803. In Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis; Springer: Berlin, Germany, 2008; pp. 1399–1402.
Tang, Y.; Li, S.; Qiao, J.; Wang, H.; Li, L. Synergistic effects of nano-sized titanium dioxide and zinc on the photosynthetic capacity and survival of Anabaena sp. Int. J. Mol. Sci. 2013, 14, 14395–14407.
Kang, N.K.; Lee, B.; Choi, G.G.; Moon, M.; Park, M.S.; Lim, J.K.; Yang, J.W. Enhancing lipid productivity of Chlorella vulgaris using oxidative stress by TiO2 nanoparticles. Korean J. Chem. Eng. 2014, 31, 861–867.
Gong, N.; Shao, K.; Feng, W.; Lin, Z.; Liang, C.; Sun, Y. Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 2011, 83, 510–516.
Polonini, H.C.; Brandao, H.M.; Raposo, N.R.B.; Brandao, M.A.F.; Mouton, L.; Coute, A.; Yepremian, C.; Sivry, Y.; Brayner, R. Size-dependent ecotoxicity of barium titanate particles: The case of Chlorella vulgaris green algae. Ecotoxicology 2015, 24, 938–948.
Ksiazyk, M.; Asztemborska, M.; Steborowski, R.; Bystrzejewska-Piotrowska, G. Toxic effect of silver and platinum nanoparticles toward the freshwater microalga Pseudokirchneriella subcapitata. Bull. Environ. Contam. Toxicol. 2015, 94, 554–558.
Blaby-Haas, C.E.; Merchant, S.S. The ins and outs of algal metal transport. Biochim. Biophys. Acta 2012, 1823, 1531–1552.
Cassier-Chauvat, C.; Chauvat, F. Responses to oxidative and heavy metal stresses in cyanobacteria: Recent advances. Int. J. Mol. Sci. 2015, 16, 871–886.
Perales-Vela, H.V.; Pena-Castro, J.M.; Canizares-Villanueva, R.O. Heavy metal detoxification in eukaryotic microalgae. Chemosphere 2006, 64, 1–10.
Sears, M.E. Chelation: Harnessing and enhancing heavy metal detoxification—A review. Sci. World J. 2013, doi:10.1155/2013/219840.
Nakanishi, K.; Deuchi, K. Culture of a high-chlorophyll-producing and halotolerant Chlorella vulgaris. J. Biosci. Bioeng. 2014, 117, 617–619.
Guesmi, A.; Ladhari, N.; Hamadi, N.B.; Msaddek, M.; Sakli, F. First application of chlorophyll-a as biomordant: Sonicator dyeing of wool with betanin dye. J. Clean. Prod. 2013, 39, 97–104.
Park, S.J.; Park, Y.M. Eco-dyeing and antimicrobial properties of chlorophyllin copper complex extracted from Sasa veitchii. Fibers Polym. 2010, 11, 357–362.
Kupper, H.; Kupper, F.; Spiller, M. Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J. Exp. Bot. 1996, 47, 259–266.
Droupadi, P.R.; Krishnan, V. An efficient method of preparation of pheophytin a—Divalent metal pheophytinates. Proc. Indian Acad. Sci. 1984, 93, 117–124.
Karcz, D.; Boroń, B.; Matwijczuk, A.; Furso, J.; Staroń, J.; Ratuszna, A.; Fiedor, L. Lessons from chlorophylls: Modifications of porphyrinoids towards optimized solar energy conversion. Molecules 2014, 19, 15938–15954.
Moreira, L.M.; Lima, A.; Soares, R.R.S.; Batistela, V.R.; Gerola, A.P.; Hioka, N.; Bonacin, J.A.; Severino, D.; Baptista, M.S.; da Hora Machado, A.E. et al. Metallochlorophylls of magnesium, copper and zinc: Evaluation of the influence of the first coordination sphere on their solvatochromism and aggregation properties. J. Braz. Chem. Soc. 2009, 20, 1653–1658.
Petrovic, J.; Nikolic, G.; Markovic, D. In vitro complexes of copper and zinc with chlorophyll. J. Serb. Chem. Soc. 2006, 71, 501–512.
Ngo, T.; Zhao, Y. Formation of zinc-chlorophyll-derivative complexes in thermally processed green pears (Pyruscommunis L.). J. Food Sci. 2007, 72, 397–404.
Takaichi, S. Carotenoids in algae: Distributions, biosyntheses and functions. Mar. Drugs 2011, 9, 1101–1118.
Shukla, M.K.; Tripathi, R.D.; Sharma, N.; Dwivedi, S.; Mishra, S.; Singh, R.; Shukla, O.P.; Rai, U.N. Responses of cyanobacterium Anabaena doliolum during nickel stress. J. Environ. Biol. 2009, 30, 871–876.
Basaca-Loya, G.A.; Valdez, M.A.; Enriquez-Guevara, E.A.; Gutierrez-Millan, L.E.; Burboa, M.G. Extraction and purification of B-phycoerythrin from the red microalga Rhodosorus marinus. Cienc. Mar. 2009, 35, 359–368.
Mishra, S.K.; Shrivastav, A.; Maurya, R.R.; Patidar, S.K.; Haldar, S.; Mishra, S. Effect of light quality on the C-phycoerythrin production in marine cyanobacteria Pseudanabaena sp. isolated from Gujarat coast, India. Protein Expr. Purif. 2012, 81, 5–10.
Mortensen, A. Carotenoids and other pigments as natural colorants. Pure Appl. Chem. 2006, 8, 1477–1491.
Stahl, W.; Sies, H. Bioactivity and protective effects of natural carotenoids. Biochim. Biophys. Acta 2005, 1740, 101–107.
Kuddus, M.; Singh, P.; Thomas, G.; Al-Hazimi, A. Recent developments in production and biotechnological applications of c-phycocyanin. Biomed Res. Int. 2013, doi:10.1155/2013/742859.
Ratha, S.K.; Prasanna, R.; Gupta, V.; Dhar, D.W.; Saxena, A.K. Bioprospecting and indexing the microalgal diversity of different ecological habitats of India. World J. Microbiol. Biotechnol. 2012, 28, 1657–1667.
Kosakowska, A.; Lewandowska, J.; Ston, J.; Burkiewicz, K. Qualitative and quantitative composition of pigments in Phaeodactylum tricornutum (Bacillariophyceae) stressed by iron. BioMetals 2004, 17, 45–52.
Zapata, M.; Fraga, S.; Rodriguez, F.; Garrido, J.L. Pigment-based chloroplast types in dinoflagellates. Mar. Ecol. Prog. Ser. 2012, 465, 33–52.
Mohr, R.; Voβ, B.; Schliep, M.; Kurz, T.; Maldener, I.; Adams, D.G.; Larkum, A.D.W.; Chen, M.; Hess, W.R. A new chlorophyll d-containing cyanobacterium: Evidence for niche adaptation in the genus Acaryochloris. ISME J. 2010, 4, 1456–1469.
Chen, M.; Li, Y.; Birch, D.; Willows, R.D. A cyanobacterium that contains chlorophyll f—A red-absorbing photopigment. FEBS Lett. 2012, 586, 3249–3254.
Garbayo, I.; Cuaresma, M.; Vılchez, C.; Vega, J.M. Effect of abiotic stress on the production of lutein and β-carotene by Chlamydomonas acidophila. Process Biochem. 2008, 43, 1158–1161.
Garbayo, I.; Torronteras, R.; Forjan, E.; Cuaresma, M.; Casal, C.; Mogedas, B.; Ruiz-Domınguez, M.C.; Marquez, C.; Vaquero, I.; Fuentes-Cordero, J.L. et al. Identification and physiological aspects of a novel carotenoid-enriched, metal-resistant microalga isolated from an acidic river in Huelva (Spain). J. Phycol. 2012, 48, 607–614.
Mojaat, M.; Pruvost, J.; Foucault, A.; Legrand, J. Effect of organic carbon sources and Fe2+ ions on growth and β-carotene accumulation by Dunaliella salina. Biochem. Eng. J. 2008, 39, 177–184.
Bhattacharya, P.; Pal, R. Scope of phycoremediation of Arsenic using Phormidium tenue with special reference to modulation in cellular biochemistry. J. Algal Biomass Util. 2012, 3, 1–8.
Arunakumara, K.K.I.U.; Xuecheng, Z. Effects of heavy metals (Pb2+ and Cd2+) on the ultrastructure, growth and pigment contents of the unicellular cyanobacterium Synechocystis sp. PCC 6803. Chin. J. Oceanol. Limnol. 2009, 27, 383–388.
Arunakumara, K.K.I.U.; Xuecheng, Z.; Xiaojin, S. Bioaccumulation of Pb2+ and its effects on growth, morphology and pigment contents of Spirulina (Arthrospira) platensis. J. Ocean Univ. Chin. 2008, 7, 397–403.
Shanab, S.; Essa, A.; Shalaby, E. Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal. Behav. 2012, 7, 1–8.
Yang, F.; Wong, K.H.; Yang, Y.; Li, X.; Jiang, J.; Zheng, W.; Wu, H.; Chen, T. Purification and in vitro antioxidant activities of tellurium-containing phycobiliproteins from tellurium-enriched Spirulina platensis. Drug Des. Dev. Ther. 2014, 8, 1789–1800.
Hu, Q.; Sommerfeld, M.; Jarvis, E.; Ghirardi, M.; Posewitz, M.; Seibert, M.; Darzins, A. Microalgal triacylglycerols as feedstocks for biofuel production: Perspectives and advances. Plant J. 2008, 54, 621–639.
Luo, X.; Su, P.; Zhang, W. Advances in microalgae-derived phytosterols for functional food and pharmaceutical applications. Mar. Drugs 2015, 13, 4231–4254.
Arakaki, A.; Iwama, D.; Liang, Y.; Murakami, N.; Ishikura, M.; Tanaka, T.; Matsunaga, T. Glycosylceramides from marine green microalga Tetraselmis sp. Phytochemistry 2013, 85, 107–114.
Yilancioglu, K.; Cokol, M.; Pastirmaci, I.; Erman, B.; Cetiner, S. Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain. PLoS ONE 2014, 9, e91957.
Yang, J.S.; Cao, J.; Xing, G.L.; Yuan, H.L. Lipid production combined with biosorption and bioaccumulation of cadmium, copper, manganese and zinc by oleaginous microalgae Chlorella minutissima UTEX2341. Bioresour. Technol. 2015, 175, 537–544.
Rocchetta, I.; Mazzuca, M.; Conforti, V.; Ruiz, L.; Balzaretti, V.; Molina, M.C.R. Effect of chromium on the fatty acid composition of two strains of Euglena gracilis. Environ. Pollut. 2006, 141, 353–358.
Sun, J.; Cheng, J.; Yang, Z.; Li, K.; Zhou, J.; Cen, K. Microstructures and functional groups of Nannochloropsis sp. cells with arsenic adsorption and lipid accumulation. Bioresour. Technol. 2015, 194, 305–311.
Mohammady, N.G.-E.D.; Fathy, A.A. Humic acid mitigates viability reduction, lipids and fatty acids of Dunaliella salina and Nannochloropsis salina grown under nickel stress. Int. J. Bot. 2007, 3, 64–70.
Pinzi, S.; Rounce, P.; Herreros, J.M.; Tsolakis, A.; Dorado, M.P. The effect of biodiesel fatty acid composition on combustion and diesel engine exhaust emissions. Fuel 2013, 104, 170–182.
Islam, M.A.; Magnusson, M.; Brown, R.J.; Ayoko, G.A.; Nabi, M.N.; Heimann, K. Microalgal species selection for biodiesel production based on fuel properties derived from fatty acid profiles. Energies 2013, 6, 5676–5702.
Stansell, G.R.; Gray, V.M.; Sym, S.D. Microalgal fatty acid composition: Implications for biodiesel quality. J. Appl. Phycol. 2012, 24, 791–801.
Komprda, T. Eicosapentaenoic and docosahexaenoic acids as inflammation-modulating and lipid homeostasis influencing nutraceuticals: A review. J. Funct. Foods 2012, 4, 25–38.
Wang, M.; Kuo-Dahab, W.C.; Dolan, S.; Park, C. Kinetics of nutrient removal and expression of extracellular polymeric substances of the microalgae, Chlorella sp. and Micractinium sp., in wastewater treatment. Bioresour. Technol. 2014, 154, 131–137.
Villay, A.; Laroche, C.; Roriz, D.; Alaoui, H.E.; Delbac, F.; Michaud, P. Optimisation of culture parameters for exopolysaccharides production by the microalga Rhodella violacea. Bioresour. Technol. 2013, 146, 732–735.
Mishra, A.; Jha, B. Isolation and characterization of extracellular polymeric substances from micro-algae Dunaliella salina under salt stress. Bioresour. Technol. 2009, 100, 3382–3386.
Penna, A.; Berluti, S.; Penna, N.; Magnani, M. Influence of nutrient ratios on the in vitro extracellular polysaccharide production by marine diatoms from the Adriatic Sea. J. Plankton Res. 1999, 21, 1681–1690.
Mota, R.; Guimaraes, R.; Buttel, Z.; Rossi, F.; Colica, G.; Silva, C.J.; Santos, C.; Gales, L.; Zille, A.; de Philippis, R. et al. Production and characterization of extracellular carbohydrate polymer from Cyanothece sp. CCY 0110. Carbohydr. Polym. 2013, 92, 1408–1415.
Bafana, A. Characterization and optimization of production of exopolysaccharide from Chlamydomonas reinhardtii. Carbohydr. Polym. 2013, 95, 746–752.
Pereira, S.; Zille, A.; Micheletti, E.; Moradas-Ferreira, P.; de Philippis, R.; Tamagnini, P. Complexity of cyanobacterial exopolysaccharides: Composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol. Rev 2009, 33, 917–941.
Raposo, M.F.J.; de Morais, R.M.S.C.; Bernardo de Morais, A.M.M. Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar. Drugs 2013, 11, 233–252.
Kiran, B.; Thanasekaran, K. Metal tolerance of an indigenous cyanobacterial strain, Lyngbya putealis. Int. Biodeterior. Biodegradation 2011, 65, 1128–1132.
Miao, A.J.; Schwehr, K.A.; Xu, C.; Zhang, S.J.; Luo, Z.; Quigg, A.; Santschi, P.H. The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ. Pollut. 2009, 157, 3034–3041.
Zhang, S.J.; Jiang, Y.; Chen, C.S.; Creeley, D.; Schwehr, K.A.; Quigg, A.; Chin, W.C.; Santschi, P.H. Ameliorating effects of extracellular polymeric substances excreted by Thalassiosira pseudonana on algal toxicity of CdSe quantum dots. Aquat. Toxicol. 2013, 126, 214–223.
Goo, B.G.; Baek, G.; Choi, D.J.; Park, Y.I.; Synytsya, A.; Bleha, R.; Seong, D.H.; Lee, C.G.; Park, J.K. Characterization of a renewable extracellular polysaccharide from defatted microalgae Dunaliella tertiolecta. Bioresour. Technol. 2013, 129, 343–350.
Ahner, B.A.; Price, N.M.; Morel, F.M.M. Phytochelatin production by marine phytoplankton at low free metal ion concentrations: Laboratory studies and field data from Massachusetts Bay. Proc. Natl. Acad. Sci. USA 1994, 91, 8433–8436.
Faucheur, L.S.; Behra, R.; Sigg, L. Phytochelatin induction, cadmium accumulation, and algal sensitivity to free cadmium ion in Scenedesmus vacuolatus. Environ. Toxicol. Chem. 2005, 24, 1731–1737.
Kawakami, S.K.; Gledhill, M.; Achterberg, E.P. Effects of metal combinations on the production of phytochelatins and glutathione by the marine diatom Phaeodactylum tricornutum. BioMetals 2006, 19, 51–60.
Morelli, E.; Scarano, G. Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum. Mar. Environ. Res. 2001, 52, 383–395.
Morelli, E.; Scarano, G. Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum. Plant Sci. 2004, 167, 289–296.
Tukaj, Z.; Bascik-Remisiewicz, A.; Skowronski, T.; Tukaj, C. Cadmium effect on the growth, photosynthesis, ultrastructure and phytochelatin content of green microalga Scenedesmus armatus: A study at low and elevated CO2 concentration. Environ. Exp. Bot. 2007, 60, 291–299.
Pawlik-Skowronska, B.; Pirszel, J.; Kalinowska, R.; Skowronski, T. Arsenic availability, toxicity and direct role of GSH and phytochelatins in As detoxification in the green alga Stichococcus bacillaris. Aquat. Toxicol. 2004, 70, 201–212.
Volland, S.; Schaumloffer, D.; Dobritzsch, D.; Krauss, G.J.; Lutz-Meindl, U. Identification of phytochelatins in the cadmium-stressed conjugating green alga Micrasterias denticulata. Chemosphere 2013, 91, 448–454.
Bhargava, P.; Srivastava, A.K.; Urmil, S.; Rai, L.C. Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum. J. Plant Physiol. 2005, 162, 1220–1225.
Brautigam, A.; Bomke, S.; Pfeifer, T.; Karst, U.; Krauss, G.J.; Wesenberg, D. Quantification of phytochelatins in Chlamydomonas reinhardtii using ferrocene-based derivatization. Metallomics 2010, 2, 565–570.
Adam, V.; Zehnalek, J.; Petrlova, J.; Potesil, D.; Sures, B.; Trnkova, L.; Jelen, F.; Vitecek, J.; Kizek, R. Phytochelatin modified electrode surface as a sensitive heavy-metal ion biosensor. Sensors 2005, 5, 70–84.
Politi, J.; Spadavecchia, J.; Iodice, M.; de Stefano, L. Oligopeptide—Heavy metal interaction monitoring by hybrid gold nanoparticle based assay. Analyst 2015, 140, 149.
Thomas, J.; Ross, C.W.; Chastain, C.J.; Koomanoff, N.; Hendrix, J.E.; Volkenburgh, E.V. Cytokinin-induced wall extensibility in excised cotyledons of radish and cucumber. Plant Physiol. 1981, 68, 107–110.
Wareing, P.F.; Bradbeer, J.W. Abscisic acid as a natural growth regulator (and discussion). Philos. Trans. R. Soc. Lond. B 1978, 284, 483–498.
Rattan, S.I.S.; Sodagam, L. Gerontomodulatory and youth-preserving effects of zeatin on human skin fibroblasts undergoing aging in vitro. Rejuvenation Res. 2005, 8, 46–57.
Liu, X.; Berezniak, T.; Panek, J.J.; Jezierska-Mazzarello, A. Theoretical study of zeatin—A plant hormone and potential drug for neural diseases—On the basis of DFT, MP2 and target docking. Chem. Phys. Lett. 2013, 557, 140–144.
Kawano, T. Possible use of indole-3-acetic acid and its antagonist tryptophan betaine in controlled killing of horseradish peroxidase-labeled human cells. Med. Hypotheses 2003, 60, 664–666.
Lu, Y.; Xu, J. Phytohormones in microalgae: A new opportunity for microalgal biotechnology? Trends Plant Sci. 2015, 20, 273–282.
Bajguz, A. Suppression of Chlorella vulgaris growth by cadmium, lead, and copper stress and its restoration by endogenous brassinolide. Arch. Environ. Contam. Toxicol. 2011, 60, 406–416.
Wang, Y.; Wang, S.; Xu, P.; Liu, C.; Liu, M.; Wang, Y.; Wang, C.; Zhang, C.; Ge, Y. Review of arsenic speciation, toxicity and metabolism in microalgae. Rev. Environ. Sci. Biotechnol. 2015, doi:10.1007/s11157-015-9371-9.
Yan, C.; Wang, Z.; Luo, Z. Arsenic Efflux from Microcystis aeruginosa under different phosphate regimes. PLoS ONE 2014, 9, e116099.
Xue, X.M.; Raber, G.; Foster, S.; Chen, S.C.; Francesconi, K.A.; Zhu, Y.G. Biosynthesis of arsenolipids by the cyanobacterium Synechocystis sp. PCC 6803. Environ. Chem. 2014, 11, 506–513.
Wang, Z.; Luo, Z.; Yan, C. Accumulation, transformation, and release of inorganic arsenic by the freshwater cyanobacterium Microcystis aeruginosa. Environ. Sci. Pollut. Res. 2013, 20, 7286–7295.
Miyashita, S.I.; Fujiwara, S.; Tsuzuki, M.; Kaise, T. Rapid biotransformation of arsenate into oxo-arsenosugars by a freshwater unicellular green alga, Chlamydomonas reinhardtii. Biosci. Biotechnol. Biochem. 2011, 75, 522–530.
Miyashita, S.I.; Fujiwara, S.; Tsuzuki, M.; Kaise, T. Cyanobacteria produce arsenosugars. Environ. Chem. 2012, 9, 474–484.
Duncan, E.G.; Maher, W.A.; Foster, S.D.; Krikowa, F. The influence of arsenate and phosphate exposure on arsenic uptake, metabolism and species formation in the marine phytoplankton Dunaliella tertiolecta. Mar. Chem. 2013, 157, 78–85.
Foster, S.; Thomson, D.; Maher, W. Uptake and metabolism of arsenate by axenic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutum. Mar. Chem. 2008, 108, 172–183.
Chen, B.; Liu, Q.; Popowich, A.; Shen, S.; Yan, X.; Zhang, Q.; Li, X.F.; Weinfeld, M.; Cullen, W.R.; Le, X.C. Therapeutic and analytical applications of arsenic binding to proteins. Metallomics 2015, 7, 39.
Ju-Nam, Y.; Lead, J.R. Manufactured nanoparticles: An overview of their chemistry, interactions and potential environmental implications. Sci. Total Environ. 2008, 400, 396–414.
Tavakoli, A.; Sohrabi, M.; Kargari, A. A Review of methods for synthesis of nanostructured metals with emphasis on iron compounds. Chem. Pap. 2007, 61, 151–170.
Hulkoti, N.I.; Taranath, T.C. Biosynthesis of nanoparticles using microbes—A review. Colloids Surf. B Biointerfaces 2014, 121, 474–483.
Płaza, G.A.; Chojniak, J.; Banat, I.M. Biosurfactant mediated biosynthesis of selected metallic nanoparticles. Int. J. Mol. Sci. 2014, 15, 13720–13737.
Luangpipat, T.; Beattie, I.R.; Chisti, Y.; Haverkamp, R.G. Gold nanoparticles produced in a microalga. J. Nanopart. Res. 2011, 13, 6439–6445.
Feurtet-Mazel, A.; Mornet, S.; Charron, L.; Mesmer-Dudons, N.; Maury-Brachet, R.; Baudrimont, M. Biosynthesis of gold nanoparticles by the living freshwater diatom Eolimna minima, a species developed in river biofilms. Environ. Sci. Pollut. Res. 2015, doi:10.1007/s11356-015-4139-x.
Kadukova, J.; Velgosova, O.; Mrazikova, A.; Marcincakova, R. The effect of culture age and initial silver concentration on biosynthesis of Ag nanoparticles. Nova Biotechnol. Chim. 2014, 13, 28–37.
Patel, V.; Berthold, D.; Puranik, P.; Gantar, M. Screening of cyanobacteria and microalgae for their ability to synthesize silver nanoparticles with antibacterial activity. Biotechnol. Rep. 2014, 20, 7286–7295.
Jena, J.; Pradhan, N.; Nayak, R.R.; Dash, B.P.; Sukla, L.B.; Panda, P.K.; Mishra, B.K. Microalga Scenedesmus sp.: A potential low-cost green machine for silver nanoparticle synthesis. J. Microbiol. Biotechnol. 2014, 24, 522–533.
Eroglu, E.; Chen, X.; Bradshaw, M.; Agarwal, V.; Zou, J.; Stewart, S.G.; Duan, X.; Lamb, R.N.; Smith, S.M.; Raston, C.L. et al. Biogenic production of palladium nanocrystals using microalgae and their immobilization on chitosan nanofibers for catalytic applications. RSC Adv. 2013, 3, 1009.
Lengke, M.F.; Fleet, M.E.; Southam, G. Synthesis of palladium nanoparticles by reaction of filamentous cyanobacterial biomass with a palladium(II) chloride complex. Langmuir 2007, 23, 8982–8987.
Jena, J.; Pradhan, N.; Aishvarya, V.; Nayak, R.R.; Dash, B.P.; Sukla, L.B.; Panda, P.K.; Mishra, B.K. Biological sequestration and retention of cadmium as CdS nanoparticles by the microalga Scenedesmus-24. J. Appl. Phycol. 2014, doi:10.1007/s10811-014-0499-8.
Santomauro, G.; Srot, V.; Bussmann, B.; van Aken, P.A.; Brümmer, F.; Strunk, H.; Bill, J. Biomineralization of zinc-phosphate-based nano needles by living microalgae. J. Biomater. Nanobiotechnol. 2012, 3, 362–370.
Schulze, H.; Brand, J.J. Lead toxicity and phosphate deficiency in Chlamydomonas. Plant Physiol. 1978, 62, 727–730.
Mera, R.; Torres, E.; Abalde, J. Sulphate, more than a nutrient, protects the microalga Chlamydomonas moewusii from cadmium toxicity. Aquat. Toxicol. 2014, 148, 92–103.
Edwards, C.D.; Beatty, J.C.; Loiselle, J.B.R.; Vlassov, K.A.; Lefebvre, D.D. Aerobic transformation of cadmium through metal sulfide biosynthesis in photosynthetic microorganisms. BMC Microbiol. 2013, 13, 161.
Liu, J.; Sun, Z.; Lavoie, M.; Fan, X.; Bai, X.; Qian, H. Ammonium reduces chromium toxicity in the freshwater alga Chlorella vulgaris. Appl. Microbiol. Biotechnol. 2015, 99, 3249–3258.
Deleebeeck, N.M.E.; de Schamphelaere, K.A.C.; Janssen, C.R. Effects of Mg2+ and H+ on the toxicity of Ni2+ to the unicellular green alga Pseudokirchneriella subcapitata: Model development and validation with surface waters. Sci. Total Environ. 2009, 407, 1901–1914.
Franklin, N.M.; Stauber, J.L.; Markich, S.J.; Lim, R.P. pH-dependent toxicity of copper and uranium to a tropical freshwater alga (Chlorella sp.). Aquat. Toxicol. 2000, 48, 275–289.
Volland, S.; Bayer, E.; Baumgartner, V.; Andosch, A.; Lutz, C.; Sima, E.; Lutz-Meindl, U. Rescue of heavy metal effects on cell physiology of the algal model system Micrasterias by divalent ions. J. Plant Physiol. 2014, 171, 154–163.
Cheloni, G.; Cosio, C.; Slaveykova, V.I. Antagonistic and synergistic effects of light irradiation on the effects of copper on Chlamydomonas reinhardtii. Aquat. Toxicol. 2014, 155, 275–282.
Piotrowska-Niczyporuk, A.; Bajguz, A.; Zambrzycka, E.; Godlewska-Zylkiewicz, B. Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol. Biochem. 2012, 52, 52–65.
Ma, M.; Zhu, W.; Wang, Z.; Witkamp, G.J. Accumulation, assimilation and growth inhibition of copper on freshwater alga (Scenedesmus subspicatus 86.81 SAG) in the presence of EDTA and fulvic acid. Aquat. Toxicol. 2003, 63, 221–228.
Hao, S.; Xiaorong, W.; Liansheng, W.; Lemei, D.; Zhong, L.; Yijun, C. Bioconcentration of rare earth elements lanthanum, gadolinium and yttrium in algae (Chlorella Vulgarize Beijerinck): Influence of chemical species. Chemosphere 1997, 34, 1753–1760.
Errecalde, O.; Seidl, M.; Campbell, P.G.C. Influence of a low molecular weight metabolite (citrate) on the toxicity of cadmium and zinc to the unicellular green alga Selenastrum capricornutum: An exception to the free-ion model. Water Res. 1998, 32, 419–429.
Gerringa, L.J.A.; de Baar, H.J.W.; Timmermans, K.R. A comparison of iron limitation of phytoplankton in natural oceanic waters and laboratory media conditioned with EDTA. Mar. Chem. 2000, 68, 335–346.
Lewin, J.; Chen, C.H. Available iron: A limiting factor for marine phytoplankton. Limnol. Oceanogr. 1971, 16, 670–675.
Botebol, H.; Sutak, R.; Scheiber, I.F.; Blaiseau, P.L.; Bouget, F.Y.; Camadro, J.M.; Lesuisse, E. Different iron sources to study the physiology and biochemistry of iron metabolism in marine micro-algae. Biometals 2014, 27, 75–88.
Kean, M.A.; Brons Delgado, E.; Mensink, B.P.; Bugter, M.H.J. Iron chelating agents and their effects on the growth of Pseudokirchneriella subcapitata, Chlorella vulgaris, Phaeodactylum tricornutum and Spirulina platensis in comparison to Fe-EDTA. J. Algal Biomass Util. 2015, 6, 56–73.
Koukal, B.; Gueguen, C.; Pardos, M.; Dominik, J. Influence of humic substances on the toxic effects of cadmium and zinc to the green alga Pseudokirchneriella subcapitata. Chemosphere 2003, 53, 953–961.
Kaladharan, P.; Leela Bhai, K.S. Effect of humic acids on mercury toxicity to marine algae. Fish. Technol. 2007, 44, 93–98.
Tang, Y.; Li, S.; Lu, Y.; Li, Q.; Yu, S. The Influence of humic acid on the toxicity of nano-ZnO and Zn2+ to the Anabaena sp. Environ. Toxicol. 2014, doi:10.1002/tox.21964.
Sanchez-Marin, P.; Beiras, R. Adsorption of different types of dissolved organic matter to marine phytoplankton and implications for phytoplankton growth and Pb bioavailability. J. Plankton Res. 2011, 33, 1396–1409.
Lamelas, C.; Wilkinson, K.J.; Slaveykova, V.I. Influence of the composition of natural organic matter on Pb bioavailability to microalgae. Environ. Sci. Technol. 2005, 39, 6109–6116.
Sun, B.; Tanji, Y.; Unno, H. Influences of iron and humic acid on the growth of the cyanobacterium Anabaena circinalis. Biochem. Eng. J. 2005, 24, 195–201.
Worms, I.A.M.; Adenmatten, D.; Mieville, P.; Traber, J.; Slaveykova, V.I. Photo-transformation of pedogenic humic acid and consequences for Cd(II), Cu(II) and Pb(II) speciation and bioavailability to green microalga. Chemosphere 2015, 138, 908–915.
Parent, L.; Twiss, M.R.; Campbell, P.G.C. Influences of natural dissolved organic matter on the interaction of aluminum with the microalga Chlorella: A Test of the free-ion model of trace metal toxicity. Environ. Sci. Technol. 1996, 30, 1713–1720.
Tang, Y.; Tian, J.; Li, S.; Xue, C.; Xue, Z.; Yin, D.; Yu, S. Combined effects of graphene oxide and Cd on the photosynthetic capacity and survival of Microcystis aeruginosa. Sci. Total Environ. 2015, 532, 154–161.
Yang, W.W.; Miao, A.J.; Yang, L.Y. Cd2+ Toxicity to a green alga Chlamydomonas reinhardtii as influenced by its adsorption on TiO2 engineered nanoparticles. PLoS ONE 2012, 7, e32300.
Worms, I.A.M.; Boltzman, J.; Garcia, M.; Slaveykova, V.I. Cell-wall-dependent effect of carboxyl-CdSe/ZnS quantum dots on lead and copper availability to green microalgae. Environ. Pollut. 2012, 167, 27–33.
Bender, M.L.; Momiyama, M. Cyclodextrin Chemistry; Springer: Berlin, Germany, 1978.
Loftsson, T.; Brewster, M.E. Pharmaceutical applications of cyclodextrins. 1. Drug solubilization and stabilization. J. Pharm. Sci. 1996, 85, 1017–1025.
Zia, V.; Rajewski, R.A.; Stella, V.J. Effect of cyclodextrin charge on complexation of neutral and charged substrates: Comparison of (SBE)7M-β-CD to HP-β-CD. Pharm. Res. 2001, 18, 667–673.
Singh, M.; Sharma, R.; Banerjee, U.C. Biotechnological applications of cyclodextrins. Biotechnol. Adv. 2002, 20, 341–359.
Challa, R.; Ahuja, A.; Ali, J.; Khar, R.K. Cyclodextrins in drug delivery: An updated review. AAPS PharmSciTech 2005, 6, 329–357.
Bellia, F.; la Mendola, D.; Pedone, C.; Rizzarelli, E.; Saviano, M.; Vecchio, G. Selectively functionalized cyclodextrins and their metal complexes. Chem. Soc. Rev. 2009, 38, 2756–2781.
Meng, X.; Pan, Q.; Liu, Y. Preparation and properties of phytosterols with hydroxypropyl β-cyclodextrin inclusion complexes. Eur. Food Res. Technol. 2012, 235, 1039–1047.
Yuan, C.; Jin, Z.; Xu, X. Inclusion complex of astaxanthin with hydroxypropyl-β-cyclodextrin: UV, FTIR, 1H NMR and molecular modeling studies. Carbohydr. Polym. 2012, 89, 492–496.
Hoffman, D.R.; Anderson, P.P.; Schubert, C.M.; Gault, M.B.; Blanford, W.J.; Sandrin, T.R. Carboxymethyl-β-cyclodextrin mitigates toxicity of cadmium, cobalt and copper during naphthalene biodegradation. Bioresour. Technol. 2010, 101, 2672–2677.
Bi Fai, P.; Grant, A.; Reid, B.J. Compatibility of hydroxypropyl-β-cyclodextrin with algal toxicity bioassays. Environ. Pollut. 2009, 157, 135–140.
Gutsche, C. Calixarenes, Monographs in Supramolecular Chemistry; Stoddart, J., Ed.; The Royal Society of Chemisfry: Cambridge, UK, 1989.
Gutsche, C.D.; Iqbal, M. p-tert-Butylcalix[4]arene. Org. Synth. 1990, 68, 234–237.
Gutsche, C.D.; Dhawan, B.; Leonis, M.; Stewart, D. p-tert-Butylcalix[6]arene. Org. Synth. 1990, 68, 238–242.
Cram, D.J.; Cram, J.M. Container Molecules and Their Guests; The Royal Society of Chemistry: Cambridge, UK, 1997.
Sliwa, W.; Kozlowski, C. Calixarenes and Resorcinarenes: Synthesis, Properties and Applications; Wiley-VCH: Weinheim, Germany, 2009.
Schneider, H.J.; Güttes, D.; Schneider, U. A macrocyclic polyphenolate as receptor analogue for cholin and related ammonium compounds. Angew. Chem. Int. Ed. Engl. 1986, 25, 647–649.
Schneider, H.J.; Güttes, D.; Schneider, U. Host-guest complexes with water soluble macrocyclic polyphenolates including induced fit and simple elements of a proton pump. J. Am. Chem. Soc. 1988, 110, 6449–6454.
Casnati, A.; Sciotto, D.; Arena, G. Calixarenes 2001; Asfari, Z., Behmer, V., Harrowfield, J., Vicens, J., Eds.; Kluwer Academic Pubhshers: Dordrecht, The Netherlands, 2001; pp. 440–457.
Arena, G.; Cali, R.; Lombardo, G.G.; Rizzarelli, E.; Sciotto, D.; Ungaro, R.; Casnati, A. Water soluble calix[4]arenes. A thermodynamic investigation of proton complex formation. Supramol. Chem. 1992, 1, 19–24.
Johnson, C.P.; Atwood, J.L.; Steed, J.W.; Bauer, C.B.; Rogers, R.D. Transition metal complexes of p-sulfonatocalix[5]arene. Inorg. Chem. 1996, 35, 2602–2610.
Gangemi, C.M.A.; Pappalardo, A.; Sfrazzetto, G.T. Applications of supramolecular capsules derived from resorcin[4]arenes, calix[n]arenes and metallo-ligands: From biology to catalysis. RSC Adv. 2015, 5, 51919–51933.
Kobayashi, K.; Tominaga, M.; Asakawa, Y.; Aoyama, Y. Binding of amino acids in water to a highly electron-rich aromatic cavity of pyrogallol or resorcinol cyclic tetramer as π-base. Tetrahedron Lett. 1993, 34, 5121–5124.
Kobayashi, K.; Asakawa, Y.; Aoyama, Y. Complexation of methylammonium salts and sugar-related alcohols with resorcinol cyclic tetramer in water: An implication of the CH-π interaction on polar guest binding. Supramol. Chem. 1993, 2, 133–135.
Kobayashi, K.; Asakawa, Y.; Kato, Y.; Aoyama, Y. Complexation of hydrophobic sugars and nucleosides in water with tetrasulfonate derivatives of resorcinol cyclic tetramer having a polyhydroxy aromatic cavity: Importance of guest–host CH–π interaction. J. Am. Chem. Soc. 1992, 114, 10307–10313.
Lamartinea, R.; Tsukadab, M.; Wilson, D.; Shirata, A. Antimicrobial activity of calixarenes. C. R. Chim. 2002, 5, 163–169.
Mouradzadegun, A.; Elahi, S.; Abadast, F.; Motamedi, H. A straightforward route for covalently anchored pyridinium salt onto upper rim of c-methylcalix[4]resorcinarene with selective antibacterial activity against Gram-positive bacteria. Res. Chem. Intermed. 2015, doi:10.1007/s11164-015-2104-4.
Yoshida, N.; Ikeda, R.; Okuno, T. Identification and characterization of heavy metal-resistant unicellular alga isolated from soil and its potential for phytoremediation. Bioresour. Technol. 2006, 97, 1843–1849.
Kalinowska, R.; Pawlik-Skowronska, B. Metal resistance of soil algae (Chlorophyta) occurring in post-flotation Zn/Pb- and Cu-tailing ponds. Pol. J. Ecol. 2008, 56, 415–430.
Kalinowska, R.; Pawlik-Skowronska, B. Response of two terrestrial green microalgae (Chlorophyta, Trebouxiophyceae) isolated from Cu-rich and unpolluted soils to copper stress. Environ. Pollut. 2010, 158, 2778–2785.
Halter, D.; Casiot, C.; Heipieper, H.J.; Plewniak, F.; Marchal, M.; Simon, S.; Arsène-Ploetze, F.; Bertin, P.N. Surface properties and intracellular speciation revealed an original adaptive mechanism to arsenic in the acid mine drainage bio-indicator Euglena mutabilis. Appl. Microbiol. Biotechnol. 2012, 93, 1735–1744.
Marva, F.; Garcıa-Balboa, C.; Baselga-Cervera, B.; Costas, E. Rapid adaptation of some phytoplankton species to osmium as a result of spontaneous mutations. Ecotoxicology 2014, 23, 213–220.
Ipatova, V.I.; Spirkina, N.E.; Dmitrieva, A.G. Resistance of microalgae to colloidal silver nanoparticles. Russ. J. Plant Physiol. 2015, 62, 253–261.
Baos, R.; Garcia-Villada, L.; Agrelo, M.; Lopez-Rodas, V.; Hiraldo, F.; Costas, E. Short-term adaptation of microalgae in highly stressful environments: An experimental model analysing the resistance of Scenedesmus intermedius (Chlorophyceae) to the heavy metals mixture from the Aznalcóllar mine spill. Eur. J. Phycol. 2002, 37, 593–600.
Fathi, A.A.; Zaki, F.T.; Ibraheim, H.A. Response of tolerant and wild type strains of Chlorella vulgaris to copper with special References to copper uptake system. Protistology 2005, 4, 73–78.
Abdel-Raouf, N.; Al-Homaidan, A.A.; Ibraheem, I.B.M. Microalgae and wastewater treatment. Saudi J. Biol. Sci. 2012, 19, 257–275.
Kumar, K.S.; Dahms, H.U.; Won, E.J.; Lee, J.S.; Shin, K.H. Microalgae—A promising tool for heavy metal remediation. Ecotoxicol. Environ. Saf. 2015, 113, 329–352.
Nikookar, K.; Moradshahi, A.; Hosseini, L. Physiological responses of Dunaliella salina and Dunaliella tertiolecta to copper toxicity. Biomol. Eng. 2005, 22, 141–146.
Pistocchi, R.; Guerrini, F.; Balboni, V.; Boni, L. Copper toxicity and carbohydrate production in the microalgae Cylindrotheca fusiformis and Gymnodinium sp. Eur. J. Phycol. 1997, 32, 125–132.
Lopez, A.; Rico, M.; Santana-Casiano, J.M.; Gonzalez, A.G.; Gonzalez-Davila, M. Phenolic profile of Dunaliella tertiolecta growing under high levels of copper and iron. Environ. Sci. Pollut. Res. 2015, doi:10.1007/s11356-015-4717-y.
Chia, M.A.; Lombardi, A.T.; da Graca Gama Melao, M.; Parrish, C.C. Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquat. Toxicol. 2015, 160, 87–95.
Bossuyt, B.T.A.; Janssen, C.R. Long-term acclimation of Pseudokirchneriella subcapitata (Korshikov) Hindak to different copper concentrations: Changes in tolerance and physiology. Aquat. Toxicol. 2004, 68, 61–74.
Radzun, K.A.; Wolf, J.; Jakob, G.; Zhang, E.; Stephens, E.; Ross, I.; Hankamer, B. Automated nutrient screening system enables high-throughput optimisation of microalgae production conditions. Biotechnol. Biofuels 2015, 8, 65.
Ozkan, A.; Kinney, K.; Katz, L.; Berberoglu, H. Reduction of water and energy requirement of algae cultivation using an algae biofilm photobioreactor. Bioresour. Technol. 2012, 114, 542–548.
El-Enany, A.E.; Issa, A.A. Cyanobacteria as a biosorbent of heavy metals in sewage water. Environ. Toxicol. Pharmacol. 2000, 8, 95–101.
Harrison, E.Z.; Oakes, S.R.; Hysell, M.; Hay, A. Organic chemicals in sewage sludges. Sci. Total Environ. 2006, 367, 481–497.
Mustafa, E.M.; Phang, S.M.; Chu, W.L. Use of an algal consortium of five algae in the treatment of landfill leachate using the high-rate algal pond system. J. Appl. Phycol. 2012, 24, 953–963.
Richards, R.G.; Mullins, B.J. Using microalgae for combined lipid production and heavy metal removal from leachate. Ecol. Modell. 2013, 249, 59–67.
Napan, K.; Teng, L.; Quinn, J.C.; Wood, B.D. Impact of heavy metals from flue gas integration with microalgae production. Algal Res. 2015, 8, 83–88.
Gopalakrishnan, V.; Ramamurthy, D. Dyeing industry effluent system as lipid production medium of Neochloris sp. for biodiesel feedstock preparation. Biomed. Res. Int. 2014, doi:10.1155/2014/529560.
White, S.; Anandraj, A.; Trois, C. The effect of landfill leachate on hydrogen production in Chlamydomonas reinhardtii as monitored by PAM Fluorometry. Int. J. Hydrog. Energy 2013, 38, 14214–14222.
Borowitzka, M.A. Commercial production of microalgae: Ponds, tanks, tubes and fermenters. J. Biotechnol. 1999, 70, 313–321.
Moreno-Garrido, I.; Lubian, L.M.; Soares, A.M.V.M. Influence of cellular density on determination of EC50 in microalgal growth inhibition tests. Ecotoxicol. Environ. Saf. 2000, 47, 112–116.
Franklin, N.M.; Stauber, J.L.; Apte, S.C.; Lim R.P. Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays. Environ. Toxicol. Chem. 2002, 21, 742–751.
Zhang, W.; Tan, N.G.J.; Fu, B.; Li, S.F.Y. Metallomics and NMR-based metabolomics of Chlorella sp. reveal the synergistic role of copper and cadmium in multi-metal toxicity and oxidative stress. Metallomics 2015, doi:10.1039/c4mt00253a.
Song, L.; Qin, J.G.; Su, S.; Xu, J.; Clarke, S.; Shan, Y. Micronutrient requirements for growth and hydrocarbon production in the oil producing green alga Botryococcus braunii (Chlorophyta). PLoS ONE 2012, 7, e41459.
Liu, Z.Y.; Wang, G.C.; Zhou, B.C. Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour. Technol. 2008, 99, 4717–4722.
Dou, X.; Lu, X.H.; Lu, M.Z.; Yu, L.S.; Xue, R.; Ji, J.B. The effects of trace elements on the lipid productivity and fatty acid composition of Nannochloropis oculata. J. Renew. Energy 2013, doi:10.1155/2013/671545.
Berberoglu, H.; Jay, J.; Pilon, L. Effect of nutrient media on photobiological hydrogen production by Anabaena variabilis ATCC 29413. Int. J. Hydrog. Energy 2008, 33, 1172–1184.
Becker, L.J.M.; Meisch, H.U. Effect of vanadate and iron stress on the pigment composition of Chlorella fusca. Z. Naturforsch. 1981, 36, 207–209.
Salama, E.S.; Kabra, A.N.; Ji, M.K.; Kim, J.R.; Min, B.; Jeon, B.H. Enhancement of microalgae growth and fatty acid content under the influence of phytohormones. Bioresour. Technol. 2014, 172, 97–103.
Josephine, A.; Niveditha, C.; Radhika, A.; Shali, A.B.; Kumar, T.S.; Dharani, G.; Kirubagaran, R. Analytical evaluation of different carbon sources and growth stimulators on the biomass and lipid production of Chlorella vulgaris—Implications for biofuels. Biomass Bioenergy 2015, 75, 170–179.
Pradeep, V.; van Ginkel, S.W.; Park, S.; Igou, T.; Yi, C.; Fu, H.; Johnston, R.; Snell, T.; Chen, Y. Use of copper to selectively inhibit Brachionus calyciflorus (Predator) growth in Chlorella kessleri (Prey) mass cultures for algae biodiesel production. Int. J. Mol. Sci. 2015, 16, 20674–20684.
