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Diatoms as potential “green” nanocomposite and nanoparticle synthesizers: challenges, prospects, and future materials applications

Published online by Cambridge University Press:  08 March 2018

Nathalie Pytlik  and
Eike Brunner
Nathalie Pytlik
Affiliation:
Bioanalytical Chemistry, TU Dresden, Dresden 01062, Germany
Eike Brunner*
Affiliation:
Bioanalytical Chemistry, TU Dresden, Dresden 01062, Germany
*
Address all correspondence to Eike Brunner at [email protected]
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Abstract

Diatoms are unicellular, eukaryotic microalgae inhabiting nearly all aquatic habitats. They are famous for their micro- and nanopatterned silica-based cell walls, which are envisioned for various technologic purposes. Within this review article, we summarize recent in vivo modifications of diatom biosilica with respect to the following questions: (i) Which metals are taken up by diatoms and eventually processed into nanoparticles (NPs)? (ii) Are these NPs toxic for the diatoms and––if so––what factors influence toxicity? (iii) What is the mechanism underlying NP synthesis and subsequent metabolism? (iv) How can the obtained materials be useful for materials science?

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Prospective Articles
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MRS Communications , Volume 8 , Issue 2 , June 2018 , pp. 322 - 331
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Copyright © Materials Research Society 2018 

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References

1.Round, F.E., Crawford, R.M., and Mann, D.G.: The Diatoms (Cambridge Univ. Press, Cambridge, England, 1990).Google Scholar
2.Armbrust, V. E.: The life of diatoms in the world's oceans. Nature 459, 185 (2009).Google Scholar
3.Bowler, C., De Marino, A., and Falciatore, A.: Diatom cell division in an environmental context. Curr. Opin. Plant Biol. 13, 623 (2010).Google Scholar
4.Stonik, V. and Stonik, I.: Low-molecular-weight metabolites from diatoms: structures, biological roles and biosynthesis. Mar. Drugs 13, 3672 (2015).Google Scholar
5.Raven, P., Evert, R., and Eichhorn, S.: Biologie der Pflanzen (De Gruyter, Berlin, Germany, 2006).Google Scholar
6.Bozarth, A., Maier, U.G., and Zauner, S.: Diatoms in biotechnology: modern tools and applications. Appl. Microbiol. Biotechnol. 82, 195 (2009).CrossRefGoogle ScholarPubMed
7.Fischer, C.: Materialwissenschaftliches Potential biologischer Silikate: Zucht verschiedener Mikroalgen––Charakterisierung und Anwendung von Biosilikaten. Dissertation. TU Dresden, Dresden, Germany (2017).Google Scholar
8.Parkinson, J. and Gordon, R.: Beyond micromachining: the potential of diatoms. Nanotechnology 17, 190 (1999).Google Scholar
9.Kröger, N. and Poulsen, N.: Diatoms-from cell wall biogenesis to nanotechnology. Annu. Rev. Genet. 42, 83 (2008).Google Scholar
10.Losic, D., Mitchell, J.G., and Voelcker, N.: Diatomaceous lessons in nanotechnology and advanced materials. Adv. Mater. 21, 2974 (2009).CrossRefGoogle Scholar
11.Jeffryes, C., Campbell, J., Li, H., Jiao, J., and Rorrer, G.: The potential of diatom nanobiotechnology for applications in solar cells, batteries, and electroluminescent devices. Energy Environ. Sci. 4, 3930 (2011).Google Scholar
12.Nassif, N. and Livage, J.: From diatoms to silica-based biohybrids. Chem. Soc. Rev. 40, 849 (2011).Google Scholar
13.Zhang, D.Y., Wang, Y., Cai, J., Pan, J.F., Jiang, X.G., and Jiang, Y.G.: Bio-manufacturing technology based on diatom micro- and nanostructure. Chin. Sci. Bull. 57, 3836 (2012).Google Scholar
14.Jeffryes, C., Agathos, S.N., and Rorrer, G.: Biogenic nanomaterials from photosynthetic microorganisms. Curr. Opin. Biotechnol. 33, 23 (2015).Google Scholar
15.Ragni, R., Cicco, S.R., Vona, D., and Farinola, G.M.: Multiple routes to smart nanostructured materials from diatom microalgae: a chemical perspective. Adv. Mater. (2017). doi: 10.1002/adma.201704289.Google ScholarPubMed
16.Fang, Y., Berrigan, J.D., Cai, Y., Marder, S. R., and Sandhage, K. H.: Syntheses of nanostructured Cu- and Ni-based micro-assemblies with selectable 3-D hierarchical biogenic morphologies. J. Mater. Chem. 22, 1305 (2012).Google Scholar
17.Losic, D., Mitchell, J., and Voelcker, N.: Diatomaceous lessons in nanotechnology and advanced materials. Chem. Commun. 39, 4905 (2005).CrossRefGoogle Scholar
18.Fang, Y., Wu, Q., Dickerson, M. B., Cai, Y., Shian, S., Berrigan, J. D., Poulsen, N., Kröger, N., and Sandhage, K. H.: Protein-mediated layer-by-layer syntheses of freestanding microscale titania structures with biologically assembled 3-D morphologies. Chem. Mater. 21, 5704 (2009).Google Scholar
19.Fischer, C., Oschatz, M., Nickel, W., Leistenschneider, D., Kaskel, S., and Brunner, E.: Bioinspired carbide-derived carbons with hierarchical pore structure for the adsorptive removal of mercury from aqueous solution. Chem. Commun. 53, 4845 (2017).Google Scholar
20.Jantschke, A., Herrmann, A.-K., Lesnyak, V., Eychmueller, A., and Brunner, E.: Decoration of diatom biosilica with small (<10 nm) noble metal and semiconductor nanoparticles: assembly, characterization and applications. Chem. Asian J. 7, 85 (2012).Google Scholar
21.Jantschke, A., Fischer, C., Hensel, R., Braun, H., and Brunner, E.: Directed assembly of nanoparticles to isolated diatom valves using the non-wetting characteristics after pyrolysis. Nanoscale 6, 11637 (2014).Google Scholar
22.Fischer, C., Adam, M., Mueller, A., Sperling, E., Wustmann, M., van Pée, K.-H., Kaskel, S., and Brunner, E.: Gold nanoparticle-decorated diatom biosilica: a favorable catalyst for the oxidation of D-glucose. ACS Omega 1, 1253 (2016).Google Scholar
23.Fuhrmann, T., Landwehr, S., El Rharbi-Kucki, M., and Sumper, M.: Diatoms as living photonic crystals. Appl. Phys. B 78, 257 (2004).Google Scholar
24.Kucki, M. and Fuhrmann-Lieker, T.: Staining diatoms with rhodamine dyes: control of emission colour in photonic biocomposites. J. R. Soc. Interface 9, 727 (2012).Google Scholar
25.Poulsen, N., Berne, C., Spain, J., and Kröger, N.: Silica immobilization of an enzyme via genetic engineering of the diatom Thalassiosira pseudonana. Angew. Chem. Int. Ed. 46, 1843 (2007).CrossRefGoogle Scholar
26.Sheppard, V.C., Scheffel, A., Poulsen, N., and Kröger, N.: Live diatom silica immobilization of multimeric and redox-active enzymes. Appl. Environ. Microbiol. 78, 211 (2012).Google Scholar
27.Hildebrand, M., Volcani, B.E., Gassmann, W., and Schroeder, J.I.: A gene family of silicon transporters. Nature 385, 688 (1997).Google Scholar
28.Hildebrand, M., Alverson, A. J., and Thamatrakoln, K.: Comparative sequence analysis of diatom silicon transporters: toward a mechanistic model of silicon transport. J. Phycol. 42, 822 (2006).Google Scholar
29.Azam, F., Hemmingsen, B.B., and Volcani, B. E.: Germanium incorporation into the silica of diatom cell walls. Arch. Mikrobiol. 92, 11 (1973).Google Scholar
30.Davis, A.K. and Hildebrand, M.: A self-propagating system for Ge incorporation into nanostructured silica. Chem. Commun. 37, 4495 (2008).Google Scholar
31.Jeffryes, C., Gutu, T., Jiao, J., and Rorrer, G. L.: Two-stage photobioreactor process for the metabolic insertion of nanostructured germanium into the silica microstructure of the diatom Pinnularia sp. Mater. Sci. Eng. C 28, 107 (2008).Google Scholar
32.Jeffryes, B. C., Solanki, R., Rangineni, Y., Wang, W., Chang, C., and Rorrer, G. L.: Electroluminescence and photoluminescence from nanostructured diatom frustules containing metabolically inserted germanium. Adv. Mater. 20, 2633 (2008).Google Scholar
33.Ali, D. M., Divya, C., Gunasekaran, M., and Thajuddin, N.: Biosynthesis and characterization of silicon-germanium oxide nanocomposite by diatom. Dig. J. Nanomater. Biostruct. 6, 117 (2011).Google Scholar
34.Jeffryes, C., Gutu, T., Jiao, J., and Rorrer, G. L.: Metabolic insertion of nanostructured TiO into the patterned biosilica of the diatom Pinnularia sp. by a two-stage bioreactor cultivation process. ACS Nano 2, 2103 (2008).Google Scholar
35.van Bennekom, A.J., Buma, A.G.J., and Nolting, R.F.: Dissolved aluminium in the Weddell-Scotia confluence and effect of Al on the dissolution kinetics of biogenic silica. Mar. Chem. 35, 423 (1991).Google Scholar
36.Gehlen, M., Beck, L., Calas, G., Flank, A.-M., van Bennekom, A.J., and van Beusekom, J.E.E.: Unraveling the atomic structure of biogenic silica: evidence of the structural association of Al and Si in diatom frustules. Geochim. Cosmochim. Acta 66, 1601 (2002).Google Scholar
37.Machill, S., Köhler, L., Ueberlein, S., Hedrich, R., Kunaschk, M., Paasch, S., Schulze, R., and Brunner, E.: Analytical studies on the incorporation of aluminium in the cell walls of the marine diatom Stephanopyxis turris. Biometals 26, 141 (2013).Google Scholar
38.Köhler, L., Machill, S., Werner, A., Selzer, C., Kaskel, S., and Brunner, E.: Are diatoms “Green” aluminosilicate synthesis microreactors for future catalyst production? Molecules 22, 2232 (2017).Google Scholar
39.Godinho, R.M., Cabrita, M.T., Alves, L.C., and Pinheiro, T.: Changes of the elemental distributions in marine diatoms as a reporter of sample preparation artefacts. A nuclear microscopy application. Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. Atoms 348, 265 (2015).Google Scholar
40.Ellwood, M.J. and Hunter, K.A.: The incorporation of zinc and iron into the frustule of the marine diatom Thalassiosira pseudonana. Limnol. Oceanogr. 45, 1517 (2000).CrossRefGoogle Scholar
41.Ellwood, M. J., and Hunter, K. A.: Determination of the Zn/Si ratio in diatom opal: a method for the separation, cleaning and dissolution of diatoms. Mar. Chem. 66, 149 (1999).Google Scholar
42.Kaden, J., Brückner, S. I., Machill, S., Krafft, C., Pöppl, A., and Brunner, E.: Iron incorporation in biosilica of the marine diatom Stephanopyxis turris: dispersed or clustered? Biometals 30, 71 (2017).Google Scholar
43.Peng, X., Manna, L., Yang, W., Wickham, J., Scher, E., Kadavanich, A., and Alivisatos, A. P.: Shape control of CdSe nanocrystals. Nature 404, 59 (2000).Google Scholar
44.Goesmann, H. and Feldmann, C.: Nanoparticulate functional materials. Angew. Chem. Int. Ed. 49, 1362 (2010).Google Scholar
45.Zhao, P., Li, N., and Astruc, D.: State of the art in gold nanoparticle synthesis. Coord. Chem. Rev. 257, 638 (2013).Google Scholar
46.Kagan, C. R., Lifshitz, E., Sargent, E. H., and Talapin, D. V.: Building devices from colloidal quantum dots. Science 353, 885 (2016).Google Scholar
47.Narayanan, K. B. and Sakthivel, N.: Green synthesis of biogenic metal nanoparticles by terrestrial and aquatic phototrophic and heterotrophic eukaryotes and biocompatible agents. Adv. Colloid Interface Sci. 169, 59 (2011).Google Scholar
48.Crookes-Goodson, W. J., Slocik, J. M., and Naik, R. R.: Bio-directed synthesis and assembly of nanomaterials. Chem. Soc. Rev. 37, 2403 (2008).CrossRefGoogle ScholarPubMed
49.Beattie, I. R. and Haverkamp, R. G.: Silver and gold nanoparticles in plants: sites for the reduction to metal. Metallomics 3, 628 (2011).Google Scholar
50.Gardea-Torresdey, J. L., Parson, J. G., Gomez, E., Peralta-Videa, J., Troiani, H. E., Santiago, P., and Yacarman, M. J.: Formation and growth of Au nanoparticles inside live Alfalfa plants. Nano Lett. 2, 397 (2002).Google Scholar
51.Shankar, S. S., Ahmad, A., Pasricha, R., and Sastry, M.: Bioreduction of chloroaurate ions by geranium leaves and its endophytic fungus yields gold nanoparticles of different shapes. J. Mater. Chem. 13, 1822 (2003).Google Scholar
52.Greene, B., Hosea, M., McPherson, R., Henzl, M., Alexander, M. D., and Darnall, D. W.: Interaction of gold (I) and gold (I I I) complexes with algal biomass. Environ. Sci. Technol. 20, 627 (1986).Google Scholar
53.Verma, V. C., Kharwar, R. N., and Gange, A. C.: Biosynthesis of antimicrobial silver nanoparticles by the endophytic fungus Aspergillus clavatus. Nanomedicine 5, 33 (2010).Google Scholar
54.Basavaraja, S., Balaji, S. D., Lagashetty, A., Rajasab, A. H., and Venkataraman, A.: Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium semitectum. Mater. Res. Bull. 43, 1164 (2008).Google Scholar
55.Jena, J., Pradhan, N., Nayak, R. R., Dash, B. P., Sukla, L. B., Panda, P. K., and Mishra, B. K.: Microalga Scenedesmus sp.: a potential low-cost green machine for silver nanoparticle synthesis. J. Microbiol. Biotechnol. 24, 522 (2014).Google Scholar
56.Patel, V., Berthold, D., Puranik, P., and Gantar, M.: Screening of cyanobacteria and microalgae for their ability to synthesize silver nanoparticles with antibacterial activity. Biotechnol. Rep. 5, 112 (2015).Google Scholar
57.Korbekandi, H., Iravani, S., and Abbasi, S.: Production of nanoparticles using organisms. Crit. Rev. Biotechnol. 29, 279 (2009).Google Scholar
58.Chakraborty, N., Pal, R., Ramaswami, A., Nayak, D., and Lahiri, S.: Diatom: a potential bio-accumulator of gold. J. Radioanal. Nucl. Chem. 270, 645 (2006).Google Scholar
59.Schröfel, A., Kratošová, G., Krautová, M., Dobročka, E., and Vávra, I.: Biosynthesis of gold nanoparticles using diatoms-silica-gold and EPS-gold bionanocomposite formation. J. Nanopart. Res. 13, 3207 (2011).Google Scholar
60.Roychoudhury, P., Nandi, C., and Pal, R.: Diatom-based biosynthesis of gold-silica nanocomposite and their DNA binding affinity. J. Appl. Phycol. 28, 2857 (2016).Google Scholar
61.Jena, J., Pradhan, N., Dash, B. P., Panda, P. K., and Mishra, B. K.: Pigment mediated biogenic synthesis of silver nanoparticles using diatom Amphora sp. and its antimicrobial activity. J. Saudi Chem. Soc. 19, 661 (2015).Google Scholar
62.Borase, H. P., Patil, C. D., Suryawanshi, R. K., Koli, S. H., Mohite, B. V., Benelli, G., and Patil, S. V.: Mechanistic approach for fabrication of gold nanoparticles by Nitzschia diatom and their antibacterial activity. Bioprocess Biosyst. Eng. 40, 1437 (2017).CrossRefGoogle ScholarPubMed
63.Lahr, R. H. and Vikesland, P. J.: Surface-enhanced Raman spectroscopy (SERS) cellular imaging of intracellularly biosynthesized gold nanoparticles. ACS Sustain. Chem. Eng. 2, 1599 (2014).Google Scholar
64.Pytlik, N., Kaden, J., Finger, M., Naumann, J., Wanke, S., Machill, S., and Brunner, E.: Biological synthesis of gold nanoparticles by the diatom Stephanopyxis turris and in vivo SERS analyses. Algal Res. 28, 9 (2017).Google Scholar
65.Conner, S. D. and Schmid, S. L.: Regulated portals of entry into the cell. Nature 422, 37 (2003).Google Scholar
66.Pollard, T. D., Earnshaw, W. C., Lippincott-Schwartz, J., and Johnson, G. T.: Cell Biology (Elsevier, Philadelphia, USA, 2008).Google Scholar
67.Lowe, J. S. and A. P. G.: Human Histology (Elsevier, Philadelphia, USA, 2015).Google Scholar
68.Verma, A. and Stellacci, F.: Effect of surface properties on nanoparticle––cell interactions. Small 6, 12 (2010).Google Scholar
69.Tatur, S., Maccarini, M., Barker, R., Nelson, A., and Fragneto, G.: Effect of functionalized gold nanoparticles on floating lipid bilayers. Langmuir 29, 6606 (2013).Google Scholar
70.Harush-Frenkel, O., Debotton, N., Benita, S., and Altschuler, Y.: Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochem. Biophys. Res. Commun. 353, 26 (2007).Google Scholar
71.Huefner, A., Kuan, W.-L., Barker, R. A., and Mahajan, S.: Intracellular SERS nanoprobes for distinction of different neuronal cell types. Nanoletters 13, 2463 (2013).Google Scholar
72.Verma, A., Uzun, O., Hu, Y., Hu, Y., Han, H., Watson, N., Chen, S., Irvine, D. J., and Stellacci, F.: Surface structure-regulated cell membrane penetration by monolayer protected nanoparticles. Nat. Mater. 7, 588 (2008).Google Scholar
73.Nativo, P., Prior, I. A., and Brust, M.: Uptake and intracellular fate of surface-modified gold nanoparticles. ACS Nano 2, 1639 (2008).Google Scholar
74.Sahay, G., Alakhova, D. Y., and Kabanov, A. V.: Endocytosis of nanomedicines. J. Control Release 145, 182–195 (2010).Google Scholar
75.Branco, D., Lima, A., Almeida, S. F. P., and Figueira, E.: Sensitivity of biochemical markers to evaluate cadmium stress in the freshwater diatom Nitzschia palea (Kützing) W. Smith. Aquat. Toxicol. 99, 109 (2010).Google Scholar
76.Bielmyer-Fraser, G. K., Jarvis, T. A., Lenihan, H. S., and Miller, R. J.: Cellular partitioning of nanoparticulate versus dissolved metals in marine phytoplankton. Environ. Sci. Technol. 48, 13443 (2014).Google Scholar
77.Miao, A.-J. and Wang, W. X.: Predicting copper toxicity with its intracellular or subcellular concentration and the thiol synthesis in a marine diatom. Environ. Sci. Technol. 41, 1777 (2007).Google Scholar
78.Pletikapić, G., Žutić, V., Vrček, I.V., and Svetličić, V.: Atomic force microscopy characterization of silver nanoparticles interactions with marine diatom cells and extracellular polymeric substance. J. Mol. Recognit. 25, 309 (2012).Google Scholar
79.Feurtet-Mazel, A., Mornet, S., Charron, L., Mesmer-Dudons, N., Maury-Brachet, R., and Baudrimont, M.: Biosynthesis of gold nanoparticles by the living freshwater diatom Eolimna minima, a species developed in river biofilms. Environ. Sci. Pollut. Res. 23, 4334 (2016).Google Scholar
80.Peng, X., Palma, S., Fisher, N. S., and Wong, S. S.: Effect of morphology of ZnO nanostructures on their toxicity to marine algae. Aquat. Toxicol. 102, 186 (2011).Google Scholar
81.Torres, E., Cid, A., Herrero, C., and Abalde, J.: Effect of cadmium in growth, ATP content, carbon fixation and ultrastructure in the marine diatom Phaeodactylum tricornutum Bohlin. Water Air Soil Pollut. 117, 1 (2000).Google Scholar
82.Chang, Y.-N., Zhang, M., Xia, L., Zhang, J., and Xing, G.: The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials (Basel) 5, 2850 (2012).Google Scholar
83.García-Negrete, C. A., Blasco, J., Volland, M., Rojas, T. C., Hampel, M., Lapresta-Fernández, A., De Haro, M. C. J., Soto, M., and Fernández, A.: Behaviour of Au-citrate nanoparticles in seawater and accumulation in bivalves at environmentally relevant concentrations. Environ. Pollut. 174, 134 (2013).Google Scholar
84.Burchardt, A. D., Carvalho, R. N., Valente, A., Nativo, P., Gilliland, D., Garc, C. P., Passarella, R., Pedroni, V., and Lettieri, T.: Effects of silver nanoparticles in diatom Thalassiosira pseudonana and cyanobacterium Synechococcus sp. Environ. Sci. Technol. 46, 11336 (2012).Google Scholar
85.Manier, N., Bado-Nilles, A., Delalain, P., Aguerre-Chariol, O., and Pandard, P.: Ecotoxicity of non-aged and aged CeO2 nanomaterials towards freshwater microalgae. Environ. Pollut. 180, 63 (2013).Google Scholar
86.Moreno-Garrido, I., Pérez, S., and Blasco, J.: Toxicity of silver and gold nanoparticles on marine microalgae. Mar. Environ. Res. 111, 60 (2015).Google Scholar
87.Bour, A., Mouchet, F., Verneuil, L., Evariste, L., Silvestre, J., Pinelli, E., and Gauthier, L.: Toxicity of CeO2 nanoparticles at different trophic levels––effects on diatoms, chironomids and amphibians. Chemosphere 120, 230 (2015).Google Scholar
88.Verneuil, L., Silvestre, J., Mouchet, F., Flahaut, E., Boutonnet, J.-C., Bourdiol, F., Bortolamiol, T., Baqué, D., Gauthier, L., and Pinelli, E.: Multi-walled carbon nanotubes, natural organic matter, and the benthic diatom Nitzschia palea: “a sticky story”. Nanotoxicology 9, 219 (2015).Google Scholar
89.Miao, A., Schwehr, K. A., Xu, C., Zhang, S., Luo, Z., Quigg, A., and Santschi, P. H.: The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ. Pollut. 157, 3034 (2009).Google Scholar
90.Clément, L., Hurel, C., and Marmier, N.: Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants––effects of size and crystalline structure. Chemosphere 90, 1083 (2013).Google Scholar
91.Taylor, P.: Ostwald ripening in emulsions. Adv. Colloid Interface Sci. 75, 107 (1998).Google Scholar
92.Thanh, N. T. K., Maclean, N., and Mahiddine, S.: Mechanisms of nucleation and growth of nanoparticles in solution. Chem. Rev. 114, 7610 (2014).Google Scholar
93.de M. Donegá, C.: Nanoparticles––Workhorses of Nanoscience (Springer, Berlin, Heidelberg, Germany, 2014).Google Scholar