Photosynthesis Research

, Volume 125, Issue 3, pp 451–471 | Cite as

Potential of carbon nanotubes in algal biotechnology

  • Maya Dimova Lambreva
  • Teresa Lavecchia
  • Esa Tyystjärvi
  • Taras Kornelievich Antal
  • Silvia Orlanducci
  • Andrea Margonelli
  • Giuseppina Rea


A critical mass of knowledge is emerging on the interactions between plant cells and engineered nanomaterials, revealing the potential of plant nanobiotechnology to promote and support novel solutions for the development of a competitive bioeconomy. This knowledge can foster the adoption of new methodological strategies to empower the large-scale production of biomass from commercially important microalgae. The present review focuses on the potential of carbon nanotubes (CNTs) to enhance photosynthetic performance of microalgae by (i) widening the spectral region available for the energy conversion reactions and (ii) increasing the tolerance of microalgae towards unfavourable conditions occurring in mass production. To this end, current understanding on the mechanisms of uptake and localization of CNTs in plant cells is discussed. The available ecotoxicological data were used in an attempt to assess the feasibility of CNT-based applications in algal biotechnology, by critically correlating the experimental conditions with the observed adverse effects. Furthermore, main structural and physicochemical properties of single- and multi-walled CNTs and common approaches for the functionalization and characterization of CNTs in biological environment are presented. Here, we explore the potential that nanotechnology can offer to enhance functions of algae, paving the way for a more efficient use of photosynthetic algal systems in the sustainable production of energy, biomass and high-value compounds.


Microalgae Photosynthesis Phytotoxicity Functionalized carbon nanotubes Nanocarriers 



Atomic force microscopy


Critical micelle concentration


Carbon nanotubes




2,6-dichlorophenol indophenol


Docosahexaenoic acid


Dextran-coated nanoceria


Density of states


Concentration inducing 50 % growth inhibition


Eicosapentaenoic acid


CNTs labelled with FITC


Fluorescein isothiocyanate


Gum Arabic


2′,7′-dichlorodihydrofluorescein diacetate


High-pressure carbon monoxide procedure for CNTs syntheses


Purified HiPCo CNTs


Raw HiPCo CNTs


Lowest observed effect concentration


Metallic SWCNTs


Multi-walled CNTs




Nitric oxide


No effect concentration


Natural organic matter


Purified CNTs synthesized via electric arc-discharge


Raw CNTs synthesized via electric arc-discharge


Poly(allylamine hydrochloride)




Polyethylene glycol


Poly-glycolic acid


Poly-lactic acid


Poly-lactic glycolic acid


ω-3 polyunsaturated fatty acids


Reactive oxygen species




Sodium cholate


Sodium dodecylbenzene sulfonate


Sodium dodecylsulfonate


Scanning electron microscopy


CNTs synthesized via CoMoCAT process and purified by acidic treatment


SWCNT conjugated with nanoceria


Single-walled CNTs


Transmission electron microscopy



AM, GR, MDL, SO, TA and TL are supported by Joint Research Project 2015-2017 between CNR-Italy and RFBR-Russia (NANOBIO project). AM, ET, GR and MDL are supported by Grant of COST Action TD1102. COST (European Cooperation in Science and Technology) is Europe’s longest-running intergovernmental framework for cooperation in science and technology funding cooperative scientific projects called ‘COST Actions’. With a successful history of implementing scientific networking projects for over 40 years, COST offers scientists the opportunity to embark upon bottom-up, multidisciplinary and collaborative networks across all science and technology domains. For more information about COST, please visit ET is also supported by Academy of Finland and by Nordic Energy Research (AquaFEED project). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Compliance with Ethical Standard

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2015_168_MOESM1_ESM.pdf (118 kb)
Supplementary material 1 (PDF 117 kb)
11120_2015_168_MOESM2_ESM.pdf (110 kb)
Supplementary material 2 (PDF 110 kb)


  1. Annesini MC, Memoli A, Petralito S (2000) Kinetics of surfactant-induced release from liposomes: a time-dependent permeability model. J Membr Sci 180:121–131. doi: 10.1016/S0376-7388(00)00524-X CrossRefGoogle Scholar
  2. Antal T, Harju E, Pihlgren L et al (2012) Use of near-infrared radiation for oxygenic photosynthesis via photon up-conversion. Int J Hydrog Energy 37:8859–8863. doi: 10.1016/j.ijhydene.2012.01.087 CrossRefGoogle Scholar
  3. Antal TK, Krendeleva TE, Tyystjarvi E (2015) Multiple regulatory mechanisms in the chloroplast of green algae: relation to hydrogen production. Photosynth Res. doi: 10.1007/s11120-015-0157-2 PubMedCentralGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi: 10.1146/annurev.arplant.55.031903.141701 PubMedCrossRefGoogle Scholar
  5. Bachilo SM, Strano MS, Kittrell C et al (2002) Structure-assigned optical spectra of single-walled carbon nanotubes. Science 298:2361–2365. doi: 10.1126/science.1078727 PubMedCrossRefGoogle Scholar
  6. Barone PW, Baik S, Heller DA, Strano MS (2005) Near-infrared optical sensors based on single-walled carbon nanotubes. Nat Mater 4:86–92. doi: 10.1038/nmat1276 PubMedCrossRefGoogle Scholar
  7. Barron AR (2011) Carbon nanomaterials. In: Barron AR (ed) Chemistry of electronic materials. American Scientific Publishers, Los Angeles, pp 297–308Google Scholar
  8. Bates K, Kostarelos K (2013) Carbon nanotubes as vectors for gene therapy: past achievements, present challenges and future goals. Adv Drug Deliv Rev 65:2023–2033. doi: 10.1016/j.addr.2013.10.003 PubMedCrossRefGoogle Scholar
  9. Bennett SW, Adeleye A, Ji Z, Keller A (2013) Stability, metal leaching, photoactivity and toxicity in freshwater systems of commercial single wall carbon nanotubes. Water Res 47:4074–4085. doi: 10.1016/j.watres.2012.12.039 PubMedCrossRefGoogle Scholar
  10. Bishop WM, Zubeck HM (2012) Evaluation of microalgae for use as nutraceuticals and nutritional supplements. J Nutr Food Sci 2:147. doi: 10.4172/2155-9600.1000147 CrossRefGoogle Scholar
  11. Blankenship RE, Chen M (2013) Spectral expansion and antenna reduction can enhance photosynthesis for energy production. Curr Opin Chem Biol 17:457–461. doi: 10.1016/j.cbpa.2013.03.031 PubMedCrossRefGoogle Scholar
  12. Boghossian A, Choi JH, Ham MH, Strano MS (2011) Dynamic and reversible self-assembly of photoelectrochemical complexes based on lipid bilayer disks, photosynthetic reaction centers, and single-walled carbon nanotubes. Langmuir 27:1599–1609. doi: 10.1021/la103469s PubMedCrossRefGoogle Scholar
  13. Boghossian A, Sen F, Gibbons BM et al (2013) Application of nanoparticle antioxidants to enable hyperstable chloroplasts for solar energy harvesting. Adv Energy Mater 3:881–893. doi: 10.1002/aenm.201201014 CrossRefGoogle Scholar
  14. Booth A, Størseth T, Altin D et al (2015) Freshwater dispersion stability of PAA-stabilised cerium oxide nanoparticles and toxicity towards Pseudokirchneriella subcapitata. Sci Total Environ 505:596–605. doi: 10.1016/j.scitotenv.2014.10.010 PubMedCrossRefGoogle Scholar
  15. Borowitzka MA (2013) High-value products from microalgaedtheir development and commercialization. J Appl Psychol 25:743–756. doi: 10.1007/s10811-013-9983-9 Google Scholar
  16. Calkins JO, Umasankar Y, O’Neill H, Ramasamy RP (2013) High photo-electrochemical activity of thylakoid–carbon nanotube composites for photosynthetic energy conversion. Energy Environ Sci 6:1891. doi: 10.1039/c3ee40634b CrossRefGoogle Scholar
  17. Carvalho AP, Silva SO, Baptista JM, Malcata FX (2011) Light requirements in microalgal photobioreactors: an overview of biophotonic aspects. Appl Microbiol Biotechnol 89:1275–1288. doi: 10.1007/s00253-010-3047-8 PubMedCrossRefGoogle Scholar
  18. Chehimi MM, Pinson J, Salmi Z (2013) Carbon nanotubes: surface modification and applications. In: Chehimi MM, Pinson J (eds) Applied surface chemistry of nanomaterials (chemistry research and applications). Nova Science Publishers, New York, pp 95–144Google Scholar
  19. Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431. doi: 10.1016/j.tplants.2011.03.011 PubMedCrossRefGoogle Scholar
  20. Chen K, Feng H, Zhang M, Wang X (2003) Nitric oxide alleviates oxidative damage in the green alga Chlorella pyrenoidosa caused by UV-B radiation. Folia Microbiol 48:389–393. doi: 10.1007/BF02931372 CrossRefGoogle Scholar
  21. Chen K, Song L, Rao B et al (2010) Nitric oxide plays a role as second messenger in the ultraviolet-B irradiated green alga Chlorella pyrenoidosa. Folia Microbiol 55:53–60. doi: 10.1007/s12223-010-0009-6 CrossRefGoogle Scholar
  22. Cherukuri TK, Tsyboulski DA, Weisman RB (2012) Length- and defect-dependent fluorescence efficiencies of individual single-walled carbon nanotubes. ASC Nano 6:843–850. doi: 10.1021/nn2043516 CrossRefGoogle Scholar
  23. Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702. doi: 10.1016/j.biotechadv.2011.05.015 PubMedCrossRefGoogle Scholar
  24. Dang X, Yi H, Ham M-H et al (2011) Virus-templated self-assembled single-walled carbon nanotubes for highly efficient electron collection in photovoltaic devices. Nat Nanotechnol 6:377–384. doi: 10.1038/NNANO.2011.50 PubMedCrossRefGoogle Scholar
  25. Dayani Y, Malmstadt N (2012) Lipid bilayers covalently anchored to carbon nanotubes. Langmuir 28:8174–8182. doi: 10.1021/la301094h PubMedCentralPubMedCrossRefGoogle Scholar
  26. De La Torre-Roche R, Hawthorne J, Deng Y et al (2013) Multiwalled carbon nanotubes and c60 fullerenes differentially impact the accumulation of weathered pesticides in four agricultural plants. Environ Sci Technol 47:12539–12547. doi: 10.1021/es4034809 CrossRefGoogle Scholar
  27. Dewi HA, Sun G, Zheng L, Lim S (2015) Interaction and charge transfer between isolated thylakoids and multi-walled carbon nanotubes. Phys Chem Chem Phys 17:3435–3440. doi: 10.1039/c4cp04575k PubMedCrossRefGoogle Scholar
  28. Ditta A (2012) How helpful is nanotechnology in agriculture? Adv Nat Sci Nanosci Nanotechnol 3:033002. doi: 10.1088/2043-6262/3/3/033002 CrossRefGoogle Scholar
  29. Dong L, Joseph KL, Witkowski CM, Craig MM (2008) Cytotoxicity of single-walled carbon nanotubes suspended in various surfactants. Nanotechnol 19:255702. doi: 10.1088/0957-4484/19/25/255702 CrossRefGoogle Scholar
  30. Dresselhaus MS, Dresselhaus G, Saito R (1995) Physics of carbon nanotubes. Carbon 33:883–891. doi: 10.1016/0008-6223(95)00017-8 CrossRefGoogle Scholar
  31. Dukovic G, Wang F, Song D et al (2005) Structural dependence of excitonic optical transitions and band-gap energies in carbon nanotubes structural. Nano Lett 5:2314–2318. doi: 10.1021/nl0518122 PubMedCrossRefGoogle Scholar
  32. Enzing C, Ploeg M, Barbosa M, Sijtsma L (2014) Microalgaebased products for the food and feed sector: an outlook for Europe. In Vigani M et al (eds), JRC scientific and policy reports.
  33. Florence AT, Attwood D (2011) Physicochemical principles of pharmacy, 5th edn. Royal Pharmaceutical Society, LondonGoogle Scholar
  34. Foresi N, Correa-Aragunde N, Parisi G et al (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830. doi: 10.1105/tpc.109.073510 PubMedCentralPubMedCrossRefGoogle Scholar
  35. Ghirardi ML (2015) Implementation of photobiological H2 production: the O2 sensitivity of hydrogenases. Photosynth Res. doi: 10.1007/s11120-015-0158-1 PubMedCentralGoogle Scholar
  36. Giraldo JP, Landry MP, Faltermeier SM et al (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13:400–408. doi: 10.1038/nmat3890 PubMedCrossRefGoogle Scholar
  37. Gogotsi Y (2006) Nanotubes and nanofibers. Taylor and Francis Group, New YorkCrossRefGoogle Scholar
  38. Grover M, Singh SR, Venkateswarlu B (2012) Nanotechnology: scope and limitations in agriculture. Int J Nanotechnol Appl 2:10–38Google Scholar
  39. Hagen A, Hertel T (2003) Quantitative analysis of optical spectra from individual single-wall carbon nanotubes. Nano Lett 3:383–388. doi: 10.1021/nl020237o CrossRefGoogle Scholar
  40. Han J-H, Paulus GLC, Maruyama R et al (2010) Exciton antennas and concentrators from core-shell and corrugated carbon nanotube filaments of homogeneous composition. Nat Mat 9:833–839. doi: 10.1038/nmat2832
  41. Hargreaves AE, Hargreaves T (2003) An overview of surfactant-based preparations used in everyday life. In: Becher P (ed) Chemical Formulation. Royal Society of Chemistry, LondonCrossRefGoogle Scholar
  42. Hartschuh A, Pedrosa HN, Novotny L, Krauss TD (2003) Simultaneous fluorescence and raman scattering from single carbon nanotubes. Science 301:1354–1357. doi: 10.1126/science.1087118 PubMedCrossRefGoogle Scholar
  43. Hlavová M, Turóczy Z, Bišová K (2015) Improving microalgae for biotechnology—from genetics to synthetic biology. Biotechnol Adv. doi: 10.1016/j.biotechadv.2015.01.009
  44. Huang X, McLean RS, Zheng M (2005) High-resolution length sorting and purification of DNA-wrapped carbon nanotubes by size-exclusion chromatography. Anal Chem 77:6225–6228. doi: 10.1021/ac0508954 PubMedCrossRefGoogle Scholar
  45. Huang H, Yuan Q, Shah JS, Misra RD (2011) A new family of folate-decorated and carbon nanotube-mediated drug delivery system: synthesis and drug delivery response. Adv Drug Deliv Rev 63:1332–1339. doi: 10.1016/j.addr.2011.04.001 PubMedCrossRefGoogle Scholar
  46. Iijima S (1991) Helical microtubules of graphitic carbon. Nature 354:56–58. doi: 10.1038/354056a0 CrossRefGoogle Scholar
  47. Jackson P, Jacobsen NR, Baun A et al (2013) Bioaccumulation and ecotoxicity of carbon nanotubes. Chem Cent J 7:154–165. doi: 10.1186/1752-153X-7-154 PubMedCentralPubMedCrossRefGoogle Scholar
  48. Jacobs CB, Peairs MJ, Venton BJ (2010) Review: carbon nanotube based electrochemical sensors for biomolecules. Anal Chim Acta 662:105–127. doi: 10.1016/j.aca.2010.01.009 PubMedCrossRefGoogle Scholar
  49. Janssen PJD, Lambreva MD, Plumeré N et al (2014) Photosynthesis at the forefront of a sustainable life. Front Chem 2:36. doi: 10.3389/fchem.2014.00036 PubMedCentralPubMedCrossRefGoogle Scholar
  50. Kempa K, Rybczynski J, Huang Z et al (2007) Carbon nanotubes as optical antennae. Adv Mater 19:421–426. doi: 10.1002/adma.200601187 CrossRefGoogle Scholar
  51. Khodakovskaya MV, de Silva K, Biris AS et al (2012) Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano 6:2128–2135. doi: 10.1021/nn204643g PubMedCrossRefGoogle Scholar
  52. Khodakovskaya MV, Kim B-S, Kim JN et al (2013) Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small 9:115–123. doi: 10.1002/smll.201201225 PubMedCrossRefGoogle Scholar
  53. King AK, Hanus MJ, Harris AT, Minett AI (2014) Nanocarbon-chlorophyll hybrids: self assembly and photoresponse. Carbon N Y 80:746–754. doi: 10.1016/j.carbon.2014.09.024 CrossRefGoogle Scholar
  54. Klumpp C, Kostarelos K, Prato M, Bianco A (2006) Functionalized carbon nanotubes as emerging nanovectors for the delivery of therapeutics. Biochim Biophys Acta 1758:404–412. doi: 10.1143/JJAP.37.L616 PubMedCrossRefGoogle Scholar
  55. Kostarelos K, Lacerda L, Pastorin G et al (2007) Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat Nanotechnol 2:108–113. doi: 10.1038/nnano.2006.209 PubMedCrossRefGoogle Scholar
  56. Kwok KW, Leung KM, Flahaut E et al (2010) Chronic toxicity of double-walled carbon nanotubes to three marine organisms: influence of different dispersion methods. Nanomed 5:951–961. doi: 10.2217/nnm.10.59 CrossRefGoogle Scholar
  57. Lahiani MH, Dervishi E, Chen J et al (2013) Impact of carbon nanotube exposure to seeds of valuable crops. ACS Appl Mater Interfaces 5:7965–7973. doi: 10.1021/am402052x PubMedCrossRefGoogle Scholar
  58. Landry MP, Vukovic L, Kruss S et al (2015) Comparative dynamics and sequence dependence of DNA and RNA binding to single walled carbon nanotubes. J Phys Chem C 119:10048–10058. doi: 10.1021/jp511448e CrossRefGoogle Scholar
  59. Li P, Liu CY, Liu H et al (2013) Protective function of nitric oxide on marine phytoplankton under abiotic stresses. Nitric Oxide Biol Chem 33:88–96. doi: 10.1016/j.niox.2013.06.007 CrossRefGoogle Scholar
  60. Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotech 24:300–309. doi: 10.1016/j.copbio.2012.08.008 PubMedCrossRefGoogle Scholar
  61. Liu Q, Chen B, Wang Q et al (2009a) Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett 9:1007–1010. doi: 10.1021/nl803083u PubMedCrossRefGoogle Scholar
  62. Liu Z, Tabakman S, Welsher K, Dai H (2009b) Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery. Nano Res 2:85–120. doi: 10.1007/s12274-009-9009-8 PubMedCentralPubMedCrossRefGoogle Scholar
  63. Long Z, Ji J, Yang K et al (2012) Systematic and quantitative investigation of the mechanism of carbon nanotubes’ toxicity toward algae. Environ Sci Technol 46:8458–8466. doi: 10.1021/es301802g PubMedCrossRefGoogle Scholar
  64. Lopez CF, Nielsen SO, Moore PB, Klein ML (2004) Understanding nature’s design for a nanosyringe. Proc Natl Acad Sci 101:4431–4434. doi: 10.1073/pnas.0400352101 PubMedCentralPubMedCrossRefGoogle Scholar
  65. Mehra NK, Mishra V, Jain NK (2014) A review of ligand tethered surface engineered carbon nanotubes. Biomaterials 35:1267–1283. doi: 10.1016/j.biomaterials PubMedCrossRefGoogle Scholar
  66. Melis A, Melnicki MR (2006) Integrated biological hydrogen production. Int J Hydr Energy 31:1563–1573. doi: 10.1016/j.ijhydene.2006.06.038 CrossRefGoogle Scholar
  67. Merchant SS, Kropat J, Liu B et al (2011) TAG You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23:352–363. doi: 10.1016/j.copbio.2011.12.001 PubMedCrossRefGoogle Scholar
  68. Merkle AC, McQuarters AB, Lehnert N (2012) Synthesis, spectroscopic analysis and photolabilization of water-soluble ruthenium(III)-nitrosyl complexes. Dalton Trans 41:8047–8059. doi: 10.1039/c2dt30464c PubMedCrossRefGoogle Scholar
  69. Misra AN, Misra M, Singh R (2010) Nitric oxide biochemistry, mode of action and signaling in plants. J Med plants Res 4:2729–2739Google Scholar
  70. Missoum K, Belgacem MN, Bras J (2013) Nanofibrillated cellulose surface modification: a review. Materials 6:1745–1766. doi: 10.3390/ma6051745 CrossRefGoogle Scholar
  71. Moore VC, Strano MS, Haroz EH et al (2003) Individually suspended single-walled carbon nanotubes in various surfactants. Nano Lett 3:1379–1382. doi: 10.1021/nl034524j CrossRefGoogle Scholar
  72. Mühlroth A, Li K, Røkke G et al (2013) Pathways of lipid metabolism in marine algae, co-expression network, bottlenecks and candidate genes for enhanced production of EPA and DHA in species of Chromista. Marine Drugs 11:4662–4697. doi: 10.3390/md11114662 PubMedCentralPubMedCrossRefGoogle Scholar
  73. Nair R, Varghese SH, Nair BG et al (2010) Nanoparticulate material delivery to plants. Plant Sci 179:154–163. doi: 10.1016/j.plantsci.2010.04.012 CrossRefGoogle Scholar
  74. Natsuki T, Tantrakarn K, Endo M (2004) Effects of carbon nanotube structures on mechanical properties. Appl Phys 79:117–124. doi: 10.1007/s00339-003-2492-y CrossRefGoogle Scholar
  75. O’Connell MJ, Bachilo SM, Huffman CB et al (2002) Band gap fluorescence from individual single-walled carbon nanotubes. Science 297:593–596. doi: 10.1126/science.1072631 PubMedCrossRefGoogle Scholar
  76. Ould-Moussa N, Safi M, Guedeau-Boudeville M-A et al (2014) In vitro toxicity of nanoceria: effect of coating and stability in biofluids. Nanotoxicology 8:799–811. doi: 10.3109/17435390.2013.831501 PubMedGoogle Scholar
  77. Paternostre MT, Roux M, Rigaud JL (1988) Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 1. Solubilization of large unilamellar liposomes (prepared by reverse-phase evaporation) by triton X-100, octyl glucoside, and sodium cholate. Biochem 27:2668–2677. doi: 10.1021/bi00408a006 CrossRefGoogle Scholar
  78. Pedrosa HN (2006) The optical properties of single-walled carbon nanotubes. Dissertation, University of RochesterGoogle Scholar
  79. Pereira MM, Mouton L, Yéprémian C et al (2014) Ecotoxicological effects of carbon nanotubes and cellulose nanofibers in Chlorella vulgaris. J Nanobiotechnol 12:15. doi: 10.1186/1477-3155-12-15 CrossRefGoogle Scholar
  80. Perez JM, Asati A, Nath S, Kaittanis C (2008) Synthesis of biocompatible dextran-coated nanoceria with pH-dependent antioxidant properties. Small 4:552–556. doi: 10.1002/smll.200700824 PubMedCrossRefGoogle Scholar
  81. Popper Z, Tuohy MG (2010) Beyond the green: understanding the evolutionary puzzle of plant and algal cell walls. Plant Physiol 153:373–383. doi: 10.1104/pp.110.158055 PubMedCentralPubMedCrossRefGoogle Scholar
  82. Popper Z, Michel G, Hervé C et al (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590. doi: 10.1146/annurev-arplant-042110-103809 PubMedCrossRefGoogle Scholar
  83. Qian H, Chen W, Li J et al (2009) The effect of exogenous nitric oxide on alleviating herbicide damage in Chlorella vulgaris. Aquat Toxicol 92:250–257. doi: 10.1016/j.aquatox.2009.02.008 PubMedCrossRefGoogle Scholar
  84. Rawat I, Kumar RR, Mutanda T, Bux F (2013) Biodiesel from microalgae: a critical evaluation from laboratory to large scale production. Appl Energy 103:444–467. doi: 10.1016/j.apenergy.2012.10.004 CrossRefGoogle Scholar
  85. Rhiem S, Riding MJ, Baumgartner W et al (2015) Interactions of multiwalled carbon nanotubes with algal cells: quantification of association, visualization of uptake, and measurement of alterations in the composition of cells. Environ Pollut 196:431–439. doi: 10.1016/j.envpol.2014.11.011 PubMedCrossRefGoogle Scholar
  86. Richard C, Balavoine F, Schultz P, Ebbesen TW, Mioskowski C (2003) Supramolecular self-assembly of lipid derivatives on carbon nanotubes. Science 300:775–778. doi: 10.1126/science.1080848 PubMedCrossRefGoogle Scholar
  87. Rodea-Palomares I, Gonzalo S, Santiago-Morales J et al (2012) An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms. Aquat Toxicol 122–123:133–143. doi: 10.1016/j.aquatox.2012.06.005 PubMedCrossRefGoogle Scholar
  88. Röhder L, Brandt T, Sigg L, Behra R (2014) Influence of agglomeration of cerium oxide nanoparticles and speciation of cerium(III) on short term effects to the green algae Chlamydomonas reinhardtii. Aquat Toxicol 152:121–130. doi: 10.1016/j.aquatox.2014.03.027 PubMedCrossRefGoogle Scholar
  89. Rőszer T (2014) Biosynthesis of nitric oxide in plants. In: Khan MN et al (eds) Nitric oxide in plants: metabolism and role in stress physiology. Springer International Publishing, Zurich, pp 17–32CrossRefGoogle Scholar
  90. Roxbury D, Tu XM, Zheng M, Jagota A (2011) Recognition ability of DNA for carbon nanotubes correlates with their binding affinity. Langmuir 27:8282–8293. doi: 10.1021/la2007793 PubMedCrossRefGoogle Scholar
  91. Safari J, Zarnegar Z (2014) Advanced drug delivery systems: nanotechnology of health design A review. J Saudi Chem Soc 18:85–99. doi: 10.1016/j.jscs.2012.12.009 CrossRefGoogle Scholar
  92. Sahoo NG, Rana S, Cho JW, Li L, Chan SH (2010) Polymer nanocomposites based on functionalized carbon nanotubes. Prog Polym Sci 35:837–867. doi: 10.1016/j.progpolymsci.2010.03.002 CrossRefGoogle Scholar
  93. Saito R, Dresselhaus G, Dresselhaus MS (1998) Physical properties of carbon nanotube, 1st edn. World Scientific Publishing Company, SingaporeCrossRefGoogle Scholar
  94. Scholes GD, Sargent EH (2014) Bioinspired materials: boosting plant biology. Nat Mater 13:329–331. doi: 10.1038/nmat3926 PubMedCrossRefGoogle Scholar
  95. Schulz MJ, Kelkar AD, Sundaresan MJ (2006) Nanoengineering of structural, functional and smart materials. CRC Press, Taylor and Francis Group, Boca RatonGoogle Scholar
  96. Schwab F, Bucheli TD, Lukhele LP et al (2011) Are carbon nanotube effects on green algae caused by shading and agglomeration? Environ Sci Technol 45:6136–6144. doi: 10.1021/es200506b PubMedCrossRefGoogle Scholar
  97. Seabra AB, Rai M, Durán N (2014) Nano carriers for nitric oxide delivery and its potential applications in plant physiological process: a mini review. J Plant Biochem Biotechnol 23:1–10. doi: 10.1007/s13562-013-0204-z CrossRefGoogle Scholar
  98. Serag MF, Kaji N, Gaillard C et al (2011a) Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells. ACS Nano 5:493–499. doi: 10.1021/nn102344t PubMedCrossRefGoogle Scholar
  99. Serag MF, Kaji N, Venturelli E et al (2011b) Functional platform for controlled subcellular distribution of carbon nanotubes. ACS Nano 5:9264–9270. doi: 10.1021/nn2035654 PubMedCrossRefGoogle Scholar
  100. Serag MF, Braeckmans K, Habuchi S et al (2012a) Spatiotemporal visualization of subcellular dynamics of carbon nanotubes. Nano Lett 12:6145–6151. doi: 10.1021/nl3029625 PubMedCrossRefGoogle Scholar
  101. Serag MF, Kaji N, Tokeshi M et al (2012b) The plant cell uses carbon nanotubes to build tracheary elements. Integr Biol 4:127–131. doi: 10.1039/c2ib00135g CrossRefGoogle Scholar
  102. Serag MF, Kaji N, Habuchi S et al (2013) Nanobiotechnology meets plant cell biology: carbon nanotubes as organelle targeting nanocarriers. RSC Adv 3:4856. doi: 10.1039/c2ra22766e CrossRefGoogle Scholar
  103. Serag MF, Kaji N, Tokeshi M, Baba Y (2015) Carbon nanotubes and modern nanoagriculture. In: Siddiqui MH et al (eds) Nanotechnology and Plant Sciences. Springer International Publishing, Zurich, pp 183–201Google Scholar
  104. Sforza E, Enzo M, Bertucco A (2014) Design of microalgal biomass production in a continuous photobioreactor: an integrated experimental and modeling approach. Chem Eng Res Des 92:1153–1162. doi: 10.1016/j.cherd.2013.08.017 CrossRefGoogle Scholar
  105. Shrestha RG, Shrestha LK, Ariga K, Abe M (2011) Reverse micelle microstructural transformations induced by surfactant molecular structure, concentration, and temperature. J Nanosci Nanotechnol 11:7665–7675. doi: 10.1166/jnn.2011.5121 PubMedCrossRefGoogle Scholar
  106. Sicard C, Perullini M, Spedalieri C et al (2011) CeO2 nanoparticles for the protection of photosynthetic organisms immobilized in silica gels. Chem Mater 23:1374–1378. doi: 10.1021/cm103253w CrossRefGoogle Scholar
  107. Siddiqui MH, Manzer H, Al-Whaibi MH, Mohammad F (2015) Nanotechnology and plant sciences nanoparticles and their impact on plants. Springer International Publishing, ZurichGoogle Scholar
  108. Singh AK, Sharma L, Mallick N (2004) Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga, Chlorella. Ecotoxicol Environ Saf 59:223–227. doi: 10.1016/j.ecoenv.2003.10.009 PubMedCrossRefGoogle Scholar
  109. Sohn EK, Chung YS, Johari SA et al (2015) Acute toxicity comparison of single-walled carbon nanotubes in various freshwater organisms. Biomed Res Int. doi: 10.1155/2015/323090 Google Scholar
  110. Solovchenko A (2015) Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell. Photosynth Res. doi: 10.1007/s11120-015-0156-3 PubMedGoogle Scholar
  111. Sonkar SK, Roy M, Babar DG, Sarkar S (2012) Water soluble carbon nano-onions from wood wool as growth promoters for gram plants. Nanoscale 4:7670–7675. doi: 10.1039/c2nr32408c PubMedCrossRefGoogle Scholar
  112. Štork F, Bačkor M, Klejdus B et al (2013) Changes of metal-induced toxicity by H2O2/NO modulators in Scenedesmus quadricauda (Chlorophyceae). Environ Sci Pollut Res Int 20:5502–5511. doi: 10.1007/s11356-013-1541-0 PubMedCrossRefGoogle Scholar
  113. Taladriz-Blanco P, Rodríguez-Lorenzo L, Sanles-Sobrido M et al (2009) SERS study of the controllable release of nitric oxide from aromatic nitrosothiols on bimetallic, bifunctional nanoparticles supported on carbon nanotubes. Appl Mater Interfaces 1:56–59. doi: 10.1021/am800141j CrossRefGoogle Scholar
  114. Tang ZK, Zhang L, Wang N et al (2001) Superconductivity in 4 angstrom single-walled carbon nanotubes. Science 292:2462–2465. doi: 10.1126/science.1060470 PubMedCrossRefGoogle Scholar
  115. Tans SJ, Verschueren ARM, Dekker C (1998) Room-temperature transistor based on a single carbon nanotube. Nature 393:49–52. doi: 10.1038/29954 CrossRefGoogle Scholar
  116. Tchoul MN, Ford WT, Lolli G et al (2007) Effect of mild nitric acid oxidation on dispersability, size, and structure of single-walled carbon nanotubes. Chem Mater 19:5765–5772. doi: 10.1021/cm071758l CrossRefGoogle Scholar
  117. Tiwari DK, Dasgupta-Schubert N, Villaseñor-Cendejas LM et al (2013) Interfacing carbon nanotubes (CNT) with plants: enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nanoagriculture. Appl Nanosci 4:577–591. doi: 10.1007/s13204-013-0236-7 CrossRefGoogle Scholar
  118. Tripathi S, Sonkar SK, Sarkar S (2011) Growth stimulation of gram (Cicer arietinum) plant by water soluble carbon nanotubes. Nanoscale 3:1176–1181. doi: 10.1039/c0nr00722f PubMedCrossRefGoogle Scholar
  119. Tyystjärvi E (2013) Photoinhibition of photosystem II. In: Jeon K (ed) International review of cell and molecular biology. Academic Press, Elsevier Inc., Oxford, pp 243–303Google Scholar
  120. Vardharajula S, Ali SZ, Tiwari PM et al (2012) Functionalized carbon nanotubes: biomedical applications. Int J Nanomed 7:5361–5374. doi: 10.2147/IJN.S35832 Google Scholar
  121. Vigani M, Parisi C, Rodriguez-Cerezo E et al (2015) Food and feed products from micro-algae: market opportunities and challenges for the EU. Trends Food Sci Tech 42(1):81–92CrossRefGoogle Scholar
  122. Wei L, Thakkar M, Chen Y et al (2010) Cytotoxicity effects of water dispersible oxidized multiwalled carbon nanotubes on marine alga, Dunaliella tertiolecta. Aquat Toxicol 100:194–201. doi: 10.1016/j.aquatox.2010.07.001 PubMedCrossRefGoogle Scholar
  123. Wen ZY, Chen F (2003) Heterotrophic production of eicosapentaenoic acid by microalgae. Biotechnol Adv 21:273–294. doi: 10.1016/S0734-9750(03)00051-X PubMedCrossRefGoogle Scholar
  124. Williams RM, Taylor HK, Thomas J et al (2014) The Effect of DNA and sodium cholate dispersed single-walled carbon nanotubes on the green algae Chlamydomonas reinhardtii. J Nanosci. doi: 10.1155/2014/419382 Google Scholar
  125. Xiong B, Zhang W, Chen L et al (2014) Effects of Pb(II) exposure on Chlorella protothecoides and Chlorella vulgaris growth, malondialdehyde, and photosynthesis-related gene transcription. Environ Toxicol 29:1346–1354. doi: 10.1002/tox.21865 PubMedGoogle Scholar
  126. Youn S, Wang R, Gao J et al (2012) Mitigation of the impact of single-walled carbon nanotubes on a freshwater green algae: Pseudokirchneriella subcapitata. Nanotoxicol 6:161–172. doi: 10.3109/17435390.2011.562329 CrossRefGoogle Scholar
  127. Zeng X, Guo X, Su G et al (2015) Bioprocess considerations for microalgal-based wastewater treatment and biomass production. Renew Sustain Energy Rev 42:1385–1392. doi: 10.1016/j.rser.2014.11.033 CrossRefGoogle Scholar
  128. Zhai Y, Zhou K, Xue Y et al (2013) Synthesis of water-soluble chitosan-coated nanoceria with excellent antioxidant properties. RSC Adv 3:6833. doi: 10.1039/c3ra22251a CrossRefGoogle Scholar
  129. Zhang J, Boghossian AA, Barone PW et al (2011) Single molecule detection of nitric oxide enabled by d(AT)15 DNA adsorbed to near infrared fluorescent single-walled carbon nanotubes. J Am Chem Soc 133:567–581. doi: 10.1021/ja1084942 PubMedCrossRefGoogle Scholar
  130. Zhang S, Jiang Y, Chen C-S et al (2012) Aggregation, dissolution, and stability of quantum dots in marine environments: importance of extracellular polymeric substances. Environ Sci Technol 46:8764–8772. doi: 10.1021/es301000m PubMedCrossRefGoogle Scholar
  131. Zhang S, Jiang Y, Chen C-S et al (2013) Ameliorating effects of extracellular polymeric substances excreted by Thalassiosira pseudonana on algal toxicity of CdSe quantum dotstances. Aquat Toxicol 126:214–223. doi: 10.1016/j.aquatox.2012.11.012 PubMedCrossRefGoogle Scholar
  132. Zheng M, Jagota A, Strano MS et al (2003) Structure-based carbon nanotube sorting by sequence-dependent DNA assembly. Science 302:1545–1548. doi: 10.1126/science.1091911 PubMedCrossRefGoogle Scholar
  133. Zhu L (2015) Biorefinery as a promising approach to promote microalgae industry: an innovative framework. Renew Sustain Energy Rev 41:1376–1384. doi: 10.1016/j.rser.2014.09.040 CrossRefGoogle Scholar
  134. Ziegler KJ, Gu Z, Peng H et al (2005) Controlled oxidative cutting of single-walled carbon nanotubes. J Am Chem Soc 127:1541–1547. doi: 10.1021/ja044537e PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Institute of Crystallography, National Research Council of ItalyMonterotondo ScaloItaly
  2. 2.Department of Chemical Science and TechnologyUniversity of Rome “Tor Vergata”RomeItaly
  3. 3.Department of Biochemistry/Molecular Plant BiologyUniversity of TurkuTurkuFinland
  4. 4.Department of Biophysics, Faculty of BiologyLomonosov Moscow State UniversityMoscowRussian Federation

Personalised recommendations