Journal of Soils and Sediments

, Volume 18, Issue 4, pp 1335–1346 | Cite as

Humic substances alter the uptake and toxicity of nanodiamonds in wheat seedlings

  • Maria G. ChernyshevaEmail author
  • Ivan Yu. Myasnikov
  • Gennadii A. Badun
  • Dmitry N. Matorin
  • Dilara T. Gabbasova
  • Andrey I. Konstantinov
  • Viktor I. Korobkov
  • Natalia A. Kulikova
Natural Organic Matter: Chemistry, Function and Fate in the Environment



Detonation synthesis nanodiamonds (ND) are among the most widely applied nanoparticles due to their low cost of production and broad scope of applications. However, the fate and behavior of NDs in the environment are largely unknown. The behavior of NDs is greatly affected by humic substances (HSs), which comprise 50 to 80 % of natural organic matter in water and soil ecosystems. The uptake of detonation NDs by wheat seedlings and its toxicity were evaluated in the presence of seven HSs of different origins, including humic acids (HA, HS fraction soluble in alkali and insoluble in acid) and fulvic acids (FA, soluble in both alkali and acid).

Materials and methods

To monitor the uptake of NDs by plants, tritium-labeled NDs were produced. Liquid scintillation spectrometry and autoradiography were used to determine the amount of NDs absorbed by plants. The photosynthetic activity of the plants was measured using light response curves.

Results and discussion

After a 24-h exposure period, the ND content in the plant roots was 1720 μg g−1. The introduction of HSs decreased the ND contents in the plant roots to 680–1570 μg g−1 (except for peat FA, for which the ND content did not differ from the blank value). The observed phenomenon was probably related mainly to the influence of HSs on the zeta potential of the NDs, which shifted from positive to negative. Based on chlorophyll fluorescence evaluation, the toxicity of NDs did not inhibit photosynthesis during illumination in the physiological range. However, NDs were slightly toxic to wheat plants under excessive light, likely due to the inhibition of electron transport between Q A and Q B and the disruption of the formation of a thylakoid transmembrane potential.


The introduction of HA in a suspension of NDs obviously reduced the inhibiting effect of the NDs; however, the mitigating activities of FA were not so apparent. Our results demonstrate the urgent need for further studies of the influences of NDs on plant growth and development.


Chlorophyll fluorescence Detonation nanodiamonds Tritium labeling Zeta potential 



The authors express their deepest appreciation of Prof. Irina Perminova (Department of Chemistry, Lomonosov Moscow State University) and her group for providing standard HS samples and their physicochemical characterization. In addition, the authors thank Associate Professor A.A. Alekseev (Ammosov North Eastern Federal University, Yakutsk) for providing us with the opportunity to conduct experiments using the MPEA—2 device.

We acknowledge financial support from the Russian Foundation of Basic Research (14-03-00280).


  1. Antal TK, Matorin DN, Ilyash LV, Volgusheva AA, Osipov VA, Konyuhov IV, Krendeleva TE, Rubin AB (2009) Probing of photosynthetic reactions in four phytoplanktonic algae with a PEA fluorometer. Photosynth Res 102:67–76CrossRefGoogle Scholar
  2. Badun GA, Chernycheva MG, Yakovlev RY, Leonidov NB, Semenenko MN, Lisichkin GV (2014) A novel approach radiolabeling detonation nanodiamonds through the tritium thermal activation method. Radiochim Acta 102:941–946CrossRefGoogle Scholar
  3. Barber SA (1984) Soil nutrient bioavailability: Mechanstic approach. John Wiley and Sons. Inc., New YorkGoogle Scholar
  4. Beck CB (2010) An introduction to plant structure and development. Cambridge University Press, Plant anatomy for the twenty-first centuryCrossRefGoogle Scholar
  5. Bulychev AA, Osipov VA, Matorin DN, Vredenberg WJ (2013) Effects of far-red light on fluorescence induction in infiltrated pea leaves under diminished ΔpH and Δφ components of the proton motive force. J Bioenerg Biomembr 45:37–45CrossRefGoogle Scholar
  6. Chernysheva M, Badun G (2011) Tritium label in studying sorption of humic substances by carbon-based nanomaterials. Eur J Chem 2:61–64CrossRefGoogle Scholar
  7. Chernysheva MG, Myasnikov IY, Badun GA (2015) Myramistin adsorption on detonation nanodiamonds in the development of drug delivery platforms. Diam Relat Mater 55:45–51CrossRefGoogle Scholar
  8. Gambardella C, Ferrando S, Gatti AM, Cataldi E, Ramoino P, Aluigi MG, Faimali M, Diaspro A, Falugi C (2015) Review: Morphofunctional and biochemical markers of stress in sea urchin life stages exposed to engineered nanoparticles. Environ Toxicol. doi: 10.1002/tox.22159 Google Scholar
  9. Girard HA, El-Kharbachi A, Garcia-Argote S, Petit T, Bergonzo P, Rousseau B, Arnault J-C (2014) Tritium labeling of detonation nanodiamonds. Chem Commun 50:2916–2918CrossRefGoogle Scholar
  10. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101:217–232CrossRefGoogle Scholar
  11. Gottschalk F, Sun TY, Nowack B (2013) Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Env Pollut 181:287–300CrossRefGoogle Scholar
  12. Herlory O, Richard P, Blanchard GF (2007) Methodology of light response curves: application of chlorophyll fluorescence to microphytobenthic biofilms. Mar Biol 153:91–101CrossRefGoogle Scholar
  13. Jośko I, Oleszczuk P, Skwarek E (2016) The bioavailability and toxicity of ZnO and Ni nanoparticles and their bulk counterparts in different sediments. J Soils Sediments 16:1798–1808. doi: 10.1007/s11368-016-1365-x
  14. Khodakovskaya M, Dervishi E, Mahmood M, Xu Y, Li Z, Watanabe F, Biris AS (2009) Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano 3:3221–3227CrossRefGoogle Scholar
  15. Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, Mclaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environm Toxicol Chem 27:1825–1851CrossRefGoogle Scholar
  16. Kovalevskii DV, Permin AB, Perminova IV, Petrosyan VS (2000) Recovery of conditions for quantitative measuring the 13C NMR spectra of humic acids. Vestnik Moskovskogo universiteta Seriya 2 Khimiya 41:39–42 (in Russian)Google Scholar
  17. Kudryavtsev AV, Perminova IV, Petrosyan VS (2000) Size-exclusion chromatographic descriptors of humic substances. Anal Chim Acta 407:193–202CrossRefGoogle Scholar
  18. Kulikova NA, Perminova IV, Badun GA, Chernysheva MG, Koroleva OV, Tsvetkova EA (2010) Estimation of uptake of humic substances from different sources by Escherichia coli cells under optimum and salt stress conditions by use of tritium-labeled humic materials. Appl Environ Microbiol 76:6223–6230CrossRefGoogle Scholar
  19. Kwak JI, An Y-J (2015) A review of the ecotoxicological effects of nanowires. Int J Environ Sci Technol 12:1163–1172CrossRefGoogle Scholar
  20. Larue C, Laurette J, Herlin-Boime N, Khodja H, Fayard B, Flank A-M, Brisset F, Carriere M (2012) Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.): influence of diameter and crystal phase. Sci Tot Environ 431:197–208CrossRefGoogle Scholar
  21. Lazár D (2009) Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal of photosynthesis. Photosynthetica 47:483–498CrossRefGoogle Scholar
  22. Lead JR, Wilkinson KJ (2006) Aquatic colloids and nanoparticles: current knowledge and future trends. Environ Chem 3:159–171CrossRefGoogle Scholar
  23. Lee CW, Mahendra S, Zodrow K, LI D, Tsai Y-C, Braam J, Alvarez PJJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675CrossRefGoogle Scholar
  24. Liang Y, Si J, Römheld V (2005) Silicon uptake and transport is an active process in Cucumis sativus. New Phytol 167:797–804CrossRefGoogle Scholar
  25. Lowe LE (1992) Studies on the nature of sulphur in peat humic acids from the Fraser river Delta, British Colombia. Sci Total Environ 113:133–145CrossRefGoogle Scholar
  26. Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Tot Environ 408:3053–3061CrossRefGoogle Scholar
  27. Mantoura RFC, Riley JP (1975) The analytical concentration of humic substances from natural waters. Anal Chim Acta 76:f97CrossRefGoogle Scholar
  28. Marcon L, Riquet F, Vicogne D, Szunerits S, Bodart J-F, Boukherroub R (2010) Cellular and in vivo toxicity of functionalized nanodiamond in Xenopus embryos. J Mater Chem 20:8064–8069CrossRefGoogle Scholar
  29. Matorin DN, Plekhanov SE, Bratkovskaya LB, Yakovleva OV, Alekseev AA (2014) The effect of phenols on the parameters of chlorophyll fluorescence and reactions of P700 in green algae Scenedesmus quadricauda. Biophysics 59:374–379CrossRefGoogle Scholar
  30. Matorin DN, Todorenko DA, Seifullina NK, Zayadan BK, Rubin AB (2013) Effect of silver nanoparticles on the parameters of chlorophyll fluorescence and P700 reaction in the green alga Chlamydomonas reinhardtii. Microbiology 82:809–814CrossRefGoogle Scholar
  31. Mchedlov-Petrossyan NO, Kamneva NN, Marynin AI, Kryshtal AP, Ōsawa E (2015) Colloidal properties and behaviors of 3 nm primary particles of detonation nanodiamonds in aqueous media. Phys Chem Chem Phys 17:16186–16203CrossRefGoogle Scholar
  32. Meléndrez MF, Cárdenas G, Arbiol J (2010) Synthesis and characterization of gallium colloidal nanoparticles. J Colloid Interface Sci 346:279–287CrossRefGoogle Scholar
  33. Oukarroum A, Perreault F, Bras S, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae. Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Safety 78:80–85CrossRefGoogle Scholar
  34. Perminova IV, Frimmel FH, Kudryavtsev AV, Kulikova NA, Abbt-Braun G, Hesse S, Petrosyan VS (2003) Molecular weight characteristics of aquatic, soil, and peat humic substances as determined by size exclusion chromatography and their statistical evaluation. Environ Sci Technol 37:2477–2485CrossRefGoogle Scholar
  35. Qi M, Liu Y, Li T (2013) Nano-TiO2 improve the photosynthesis of tomato leaves under mild heat stress. Biol Trace Elem Res 156:323–328CrossRefGoogle Scholar
  36. Stirbet A, Riznichenko GY, Rubin AB, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochem Mosc 79:291–323CrossRefGoogle Scholar
  37. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty UP (eds) Probing photosynthesis: mechanisms. Regulation and Adaptation. Taylor and Francis, London, pp. 445–483Google Scholar
  38. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313CrossRefGoogle Scholar
  39. Su Y, Zhu Y (2008) Uptake of selected PAHs from contaminated soils by rice seedlings (Oryza sativa) and influence of rhizosphere on PAH distribution. Environ Pollut 155:359–365CrossRefGoogle Scholar
  40. Tyystjärvi E, Vass I (2004) Light emission as a probe of charge separation and recombination in the photosynthetic apparatus: relation of prompt fluorescence to delayed light emission and thermoluminescence. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Springer, Berlin, pp. 363–388CrossRefGoogle Scholar
  41. Vavilin DV, Polynov VA, Matorin DN, Venediktov PS (1995) The subletal concentrations of copper stimulate photosystem II photoinhibition in Chlorella pyrenoidosa. J Plant Physiol 146:609–614CrossRefGoogle Scholar
  42. Volkov DS, Semenyuk PI, Korobov MV, Proskurnin MA (2012) Quantification of nanodiamonds in aqueous solutions by spectrophotometry and thermal lens spectrometry. J Analyt Chem 67:842–850CrossRefGoogle Scholar
  43. Wang F, Liu J (2013) Nanodiamond decorated liposomes as highly biocompatible delivery vehicles and a comparison with carbon nanotubes and graphene oxide. Nanoscale 5:12375–12382CrossRefGoogle Scholar
  44. Wang Z, Quik JTK, Song L, van den Brandhof E-J, Wouterse M, Peijnenburg WJGM (2015) Humic substances alleviate the aquatic toxicity of polyvinylpyrrolidone-coated silver nanoparticles to organisms of different trophic levels. Environ Toxicol Chem 34:1239–1245CrossRefGoogle Scholar
  45. Wraight CA, Crofts AT (1971) Delayed fluorescence and the high-energy state of chloroplasts. Eur J Biochem 19:386–397CrossRefGoogle Scholar
  46. Zhan X-H, Ma H-L, Zhou L-X, Liang J-R, Jiang T-H, Xu G-H (2010) Accumulation of phenanthrene by roots of intact wheat (Triticum aestivum L.) seedlings: passive or active uptake? BMC Plant Biol 10:52–59CrossRefGoogle Scholar
  47. Zhang X, Hu W, Li J, Tao L, Wei Y (2012) A comparative study of cellular uptake and cytotoxicity of multi-walled carbon nanotubes, graphene oxide, and nanodiamond. Toxicol Res 1:62–68CrossRefGoogle Scholar
  48. Živčák M, Brestič M, Olšovská K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum L. Plant Soil Environ 54:133–139CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Maria G. Chernysheva
    • 1
    Email author
  • Ivan Yu. Myasnikov
    • 1
  • Gennadii A. Badun
    • 1
  • Dmitry N. Matorin
    • 2
  • Dilara T. Gabbasova
    • 2
  • Andrey I. Konstantinov
    • 1
  • Viktor I. Korobkov
    • 1
  • Natalia A. Kulikova
    • 3
    • 4
  1. 1.Department of ChemistryLomonosov Moscow State UniversityMoscowRussia
  2. 2.Department of BiologyLomonosov Moscow State UniversityMoscowRussia
  3. 3.Department of Soil ScienceLomonosov Moscow State UniversityMoscowRussia
  4. 4.Bach Institute of Biochemistry, Research Center of Biotechnology of RASMoscowRussia

Personalised recommendations