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Environmental Science and Pollution Research

, Volume 24, Issue 20, pp 16673–16681 | Cite as

Fullerol C60(OH)24 nanoparticles and mycotoxigenic fungi: a preliminary investigation into modulation of mycotoxin production

  • Tihomir KovačEmail author
  • Bojan Šarkanj
  • Tomislav Klapec
  • Ivana Borišev
  • Marija Kovač
  • Ante Nevistić
  • Ivica Strelec
Research Article

Abstract

Increased use of fullerols in various fields and expected increase of their environmental spread impose the necessity for testing fullerol nanoparticles (FNP) effects on microbiota. There is little information available on the interaction of mycotoxigenic fungi and FNP, despite FNP having a great potential of modifying mycotoxin production. Namely, FNP exhibit both ROS-quenching and ROS-producing properties, while oxidative stress stimulates mycotoxin synthesis in the fungi. In order to shed some light on the extent of interaction between FNP and mycotoxigenic fungi, the effects of fullerol C60(OH)24 nanoparticles (10, 100, 1000 ng/mL) on mycelial growth, aflatoxin production and oxidative stress modulation in an aflatoxigenic strain of Aspergillus flavus (NRRL 3251) during 168 h of incubation in a liquid culture medium were examined. FNP slightly reduced mycelial biomass weight, but significantly decreased aflatoxin concentration in media. Lipid peroxide content, superoxide dismutase, catalase and glutathione peroxidase activities suggest that FNP treatments hormetically reduced oxidative stress within fungal cells in turn suppressing aflatoxin production. These findings contribute to the assessment of environmental risk and application potential of fullerols.

Keywords

Fullerol C60(OH)24 Nanoparticles Aspergillus flavus Mycelial growth Aflatoxin production Oxidative stress 

Notes

Acknowledgements

The authors would like to thank prof. dr. sc. Mirta Benšić from the Department of Mathematics, Josip Juraj Strossmayer University of Osijek, for the advice in the selection of proper statistical methods. This work was funded by Josip Juraj Strossmayer University of Osijek (young scientist grant) and partially supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. III 45005).

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2017_9214_MOESM1_ESM.pdf (284 kb)
ESM 1 (PDF 284 kb)

References

  1. Amaike S, Keller NP (2011) Aspergillus flavus. Annu Rev Phytopathol 49:107–133. doi: 10.1146/annurev-phyto-072910-095221 CrossRefGoogle Scholar
  2. Angelova MB, Pashova SB, Spasova BK, Vassilev SV, Slokoska LS (2005) Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol Res 109:150–158. doi: 10.1017/S0953756204001352 CrossRefGoogle Scholar
  3. Aoshima H, Kokubo K, Shirakawa S, Ito M, Yamana S, Oshima T (2009) Antimicrobial of fellerenes and their OH derivatives. Biocontrol Sci 14:69–72CrossRefGoogle Scholar
  4. Badireddy AR, Hotze EM, Chellam S, Alvarez P, Wiesner MR (2007) Inactivation of bacteriophages via photosensitization of fullerol nanoparticles. Environ Sci Technol 41:6627–6632. doi: 10.1021/es0708215 CrossRefGoogle Scholar
  5. Battilani P, Rossi V, Giorni P, Pietri A, Gualla A, van der Fels-Klerx H, Booij C, Moretti A, Logrieco A, Miglietta F, Toscano P, Miraglia M, De Santis B, Brera C (2012) Scientific report submitted to EFSA. Modelling, predicting and mapping the emergence of aflatoxins in cereals in the EU due to climate change. EFSA. doi: 10.1038/srep24328
  6. Bosi S, Da Ros T, Spalluto G, Prato M (2003) Fullerene derivatives: an attractive tool for biological applications. Eur J Med Chem 38:913–923. doi: 10.1016/j.ejmech.2003.09.005 CrossRefGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  8. Cai X, Jia H, Liu Z, Hou B, Luo C, Feng Z, Li W, Liu J (2008) Polyhydroxylated fullerene derivative C(60)(OH)(24) prevents mitochondrial dysfunction and oxidative damage in an MPP(+) -induced cellular model of Parkinson’s disease. J Neurosci Res 86:3622–3634. doi: 10.1002/jnr.21805 CrossRefGoogle Scholar
  9. Chanda A, Roze LV, Kang S, Artymovich KA, Hicks GR, Raikhel NV, Calvo AM, Linz JE (2009) A key role for vesicles in fungal secondary metabolism. Proc Natl Acad Sci U S A 106:19533–19538. doi: 10.1073/pnas.0907416106 CrossRefGoogle Scholar
  10. Chanda A, Roze LV, Linz JE (2010) A possible role for exocytosis in aflatoxin export in Aspergillus parasiticus. Eukaryot Cell 9:1724–1727. doi: 10.1128/EC.00118-10 CrossRefGoogle Scholar
  11. Cherepanova NP, Panina LK, Bogomolova EV, Rybalchenko OV, Spitsina NG (1997) The studying of fungi interactions with new carbon allotropic modification—Fullerens. Mikol Fitopatol 31:27–32Google Scholar
  12. Chipley JR, Uraih N (1980) Inhibition of Aspergillus growth and aflatoxin release by derivatives of benzoic acid. Appl Environ Microbiol 40:352–357Google Scholar
  13. Djordjević A, Vojínović-Miloradov M, Petranović N, Devečerski A, Lazar D, Ribar B (1998) Catalytic preparation and characterization of C60Br24. Fuller Sci Technol 6(4):689–694. doi: 10.1080/10641229809350229
  14. Djordjevic A, Srdjenovic B, Seke M, Petrovic D, Injac R, Mrdjanovic J (2015) Review of synthesis and antioxidant potential of fullerenol nanoparticles. J Nanomater 16:280. doi: 10.1155/2015/567073 Google Scholar
  15. Duncan TV (2011) Applications of nanotechnology in food packaging and food safety: barrier materials, antimicrobials and sensors. J Colloid Interface Sci 363:1–24. doi: 10.1016/j.jcis.2011.07.017 CrossRefGoogle Scholar
  16. Emri T, Pócsi I, Sezentrimai A (1997) Glutathione metabolism and protection against oxidative stress. Free Radic Biol Med 23(5):809–814CrossRefGoogle Scholar
  17. Esworthy RS, Chu FF, Doroshow JH (2005) Chapter 7 (7.1.1.-7.1.32.). In: Current protocols in toxycology. Wiley, New York, pp 7.1.1.-7.1.32Google Scholar
  18. Farré M, Pérez S, Gajda-Schrantz K, Osorio V, Kantiani L, Ginebreda A, Barceló D (2010) First determination of C60 and C70 fullerenes and N-methylfulleropyrrolidine C60 on the suspended material of wastewater effluents by liquid chromatography hybrid quadrupole linear ion trap tandem mass spectrometry. J Hydrol 383:44–51. doi: 10.1016/j.jhydrol.2009.08.016 CrossRefGoogle Scholar
  19. Foley S, Crowley C, Smaihi M, Bonfils C, Erlanger BF, Seta P, Larroque C (2002) Cellular localisation of a water-soluble fullerene derivative. Biochem Biophys Res Commun 294:116–119. doi: 10.1016/S0006-291X(02)00445-X CrossRefGoogle Scholar
  20. Fridovich I (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201:1203–1209Google Scholar
  21. Fuller KK, Ringelberg CS, Loros JJ, Dunlap JC (2013) The fungal pathogen Aspergillus fumigatus regulates growth, metabolism, and stress resistance in response to light. MBio 4:4–6. doi: 10.1128/mBio.00142-13 CrossRefGoogle Scholar
  22. Gandomi H, Misaghi A, Basti AA, Bokaei S, Khosravi A, Abbasifar A, Javan AJ (2009) Effect of Zataria multiflora Boiss. essential oil on growth and aflatoxin formation by Aspergillus flavus in culture media and cheese. Food Chem Toxicol 47:2397–2400. doi: 10.1016/j.fct.2009.05.024 CrossRefGoogle Scholar
  23. Gao J, Wang Y, Folta KM, Krishna V, Bai W, Indeglia P, Georgieva A, Nakamura H, Koopman B, Moudgil B (2011) Polyhydroxy fullerenes (fullerols or fullerenols): beneficial effects on growth and lifespan in diverse biological models. PLoS One 6:1–8. doi: 10.1371/journal.pone.0019976 Google Scholar
  24. Grebowski J, Krokosz A, Puchala M (2013) Membrane fluidity and activity of membrane ATPases in human erythrocytes under the influence of polyhydroxylated fullerene. Biochim Biophys Acta 1828:241–248. doi: 10.1016/j.bbamem.2012.09.008 CrossRefGoogle Scholar
  25. Hadduck AN, Hindagolla V, Contreras AE, Li Q, Bakalinsky AT (2010) Does aqueous fullerene inhibit the growth of Saccharomyces cerevisiae or Escherichia coli? Appl Environ Microbiol 76:8239–8242. doi: 10.1128/AEM.01925-10 CrossRefGoogle Scholar
  26. Hedayati MT, Pasqualotto AC, Warn PA, Bowyer P, Denning DW (2007) Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology 153:1677–1692. doi: 10.1099/mic.0.2007/007641-0 CrossRefGoogle Scholar
  27. Hong SY, Linz JE, Roze LV (2013) Oxidative stress-related transcription factors in the regulation of secondary metabolism. Toxins 5:683–702. doi: 10.3390/toxins5040683 CrossRefGoogle Scholar
  28. Isakovic A (2006) Distinct cytotoxic mechanisms of pristine versus hydroxylated fullerene. Toxicol Sci 91:173–183. doi: 10.1093/toxsci/kfj127 CrossRefGoogle Scholar
  29. Jayashree T, Subramanyam C (2000) Oxidative stress a prerequisite for aflatoxin production by Aspergillus parasiticus. Free Radic Biol Med 29:981–985CrossRefGoogle Scholar
  30. Johnson-Lyles DN, Peifley K, Lockett S, Neun BW, Hansen M, Clogston J, Stern ST, McNeil SE (2010) Fullerenol cytotoxicity in kidney cells is associated with cytoskeleton disruption, autophagic vacuole accumulation, and mitochondrial dysfunction. Toxicol Appl Pharmacol 248:249–258. doi: 10.1016/j.taap.2010.08.008 CrossRefGoogle Scholar
  31. Klich MA (2007) Aspergillus flavus: the major producer of aflatoxin. Mol Plant Pathol 8:713–722. doi: 10.1111/j.1364-3703.2007.00436.x CrossRefGoogle Scholar
  32. Kovač T, Kovač M, Strelec I, Nevistić A, Molnar M (2017) Antifungal and antiaflatoxigenic activities of coumarinyl thiosemicarbazides against Aspergillus flavus NRRL 3251. Arh Hig Rada Toksikol 68:9–15. doi: 10.1515/aiht-2017-68-2883 Google Scholar
  33. Li Q, McNeil B, Harvey LM (2008) Adaptive response to oxidative stress in the filamentous fungus Aspergillus niger B1-D. Free Radic Biol Med 44:394–402. doi: 10.1016/j.freeradbiomed.2007.09.019 CrossRefGoogle Scholar
  34. Li Q, Harvey LM, McNeil B (2009) Oxidative stress in industrial fungi. Crit Rev Biotechnol 29:199–213. doi: 10.1080/07388550903004795 CrossRefGoogle Scholar
  35. Lushchak VI, Gospodaryov DV (2005) Catalases protect cellular proteins from oxidative modification in Saccharomyces cerevisiae. Cell Biol Int 29:187–192. doi: 10.1016/j.cellbi.2004.11.001 CrossRefGoogle Scholar
  36. Marković Z, Trajković V (2008) Biomedical potential of the reactive oxygen species generation and quenching by fullerenes (C60). Biomaterials 29:3561–3573. doi: 10.1016/j.biomaterials.2008.05.005 CrossRefGoogle Scholar
  37. Michiels C, Raes M, Toussaint O, Remacle J (1994) Importance of se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic Biol Med 17:235–248. doi: 10.1016/0891-5849(94)90079-5 CrossRefGoogle Scholar
  38. Mirkov SM, Djordjevic AN, Andric NL, Andric SA, Kostic TS, Bogdanovic GM, Vojinovic-Miloradov MB, Kovacevic RZ (2004) Nitric oxide-scavenging activity of polyhydroxylated fullerenol, C60(OH)24. Nitric Oxide - Biol Chem 11:201–207. doi: 10.1016/j.niox.2004.08.003 CrossRefGoogle Scholar
  39. Miskei M, Karányi Z, Pócsi I (2009) Annotation of stress-response proteins in the aspergilli. Fungal Genet Biol 46(Suppl 1):S105–S120. doi: 10.1016/j.fgb.2008.07.013 CrossRefGoogle Scholar
  40. Monticelli L, Salonen E, Ke PC, Vattulainen I (2009) Effects of carbon nanoparticles on lipid membranes: a molecular simulation perspective. Soft Matter 5:4433. doi: 10.1039/b912310e CrossRefGoogle Scholar
  41. Narasaiah KV, Sashidhar RB, Subramanyam C (2006) Biochemical analysis of oxidative stress in the production of aflatoxin and its precursor intermediates. Mycopathologia 162:179–189. doi: 10.1007/s11046-006-0052-7 CrossRefGoogle Scholar
  42. Pickering KD, Wiesner MR (2005) Fullerol-sensitized production of reactive oxygen species in aqueous solution. Environ Sci Tehnol 39:1359–1365CrossRefGoogle Scholar
  43. Plauth A, Giekowski A, Cichon S, Wowro SJ, Liedgens L, Rousseau M, Weidner C, Fuhr L, Kliem M, Jenkins G, Lotito S, Wainwright LJ, Sauer S (2016) Hormetic shifting of redox environment by pro-oxidative resveratrol protects cells against stress. Free Radical Bio Med 99:608–622. doi: 10.1016/j.freeradbiomed.2016.08.006 CrossRefGoogle Scholar
  44. Pycke BFG, Chao T-C, Herckes P, Westerhoff P, Halden RU (2012) Beyond nC60: strategies for identification of transformation products of fullerene oxidation in aquatic and biological samples. Anal Bioanal Chem 404:2583–2595. doi: 10.1007/s00216-012-6090-8 CrossRefGoogle Scholar
  45. Qiao R, Roberts AP, Mount AS, Klaine SJ (2007) Translocation of C60 and its derivatives across a lipid bilayer. Nano 7:614–619. doi: 10.1021/nl062515f Google Scholar
  46. Ratnikova TA, Govindan PN, Salonen E, Ke PC (2011) In vitro polymerization of microtubules with a fullerene derivative. ACS Nano 5:6306–6314. doi: 10.1021/nn201331n CrossRefGoogle Scholar
  47. Reverberi M, Fabbri AA, Zjalic S, Ricelli A, Punelli F, Fanelli C (2005) Antioxidant enzymes stimulation in Aspergillus parasiticus by Lentinula edodes inhibits aflatoxin production. Appl Microbiol Biotechnol 69:207–215. doi: 10.1007/s00253-005-1979-1 CrossRefGoogle Scholar
  48. Reverberi M, Zjalic S, Ricelli A, Fabbri A, Fanelli C (2006) Oxidant/antioxidant balance in Aspergillus parasiticus affects aflatoxin biosynthesis. Mycotoxin Res 22:39–47. doi: 10.1007/BF02954556 CrossRefGoogle Scholar
  49. Reverberi M, Zjalic S, Ricelli A, Punelli F, Camera E, Fabbri C, Picardo M, Fanelli C, Fabbri AA (2008) Modulation of antioxidant defense in Aspergillus parasiticus is involved in aflatoxin biosynthesis: a role for the ApyapA gene. Eukaryot Cell 7:988–1000. doi: 10.1128/EC.00228-07 CrossRefGoogle Scholar
  50. Reverberi M, Ricelli A, Zjalic S, Fabbri AA, Fanelli C (2010) Natural functions of mycotoxins and control of their biosynthesis in fungi. Appl Microbiol Biotechnol 87:899–911. doi: 10.1007/s00253-010-2657-5 CrossRefGoogle Scholar
  51. Reverberi M, Punelli M, Smith CA, Zjalić S, Scarpari M, Scala V, Cardinali G, Aspite N, Pinzari F, Payne GA, Fabbri AA, Fanelli C (2012) How peroxisomes affect aflatoxin biosynthesis in Aspergillus flavus. PLoS One 7:e48097. doi: 10.1371/journal.pone.0048097 CrossRefGoogle Scholar
  52. Roze LV, Hong S-Y, Linz JE (2013) Aflatoxin biosynthesis: current frontiers. Annu Rev Food Sci Technol 4:293–311. doi: 10.1146/annurev-food-083012-123702 CrossRefGoogle Scholar
  53. Sanchís J, Berrojalbiz N, Caballero G, Dachs J, Farré M, Barceló D (2012) Occurrence of aerosol-bound fullerenes in the Mediterranean sea atmosphere. Environ Sci Technol 46:1335–1343. doi: 10.1021/es200758m CrossRefGoogle Scholar
  54. Sanchís J, Božović D, Al-Harbi NA, Silva LF, Farré M, Barceló D (2013) Quantitative trace analysis of fullerenes in river sediment from Spain and soils from Saudi Arabia. Anal Bioanal Chem 405:5915–5923. doi: 10.1007/s00216-013-6924-z CrossRefGoogle Scholar
  55. Šarkanj B, Molnar M, Čačić M, Gille L (2013) 4-Methyl-7-hydroxycoumarin antifungal and antioxidant activity enhancement by substitution with thiosemicarbazide and thiazolidinone moieties. Food Chem 139:488–495. doi: 10.1016/j.foodchem.2013.01.027 CrossRefGoogle Scholar
  56. Schreiner KM, Filley TR, Blanchette RA, Bowen BB, Bolskar RD, Hockaday WC, Masiello CA, Raebiger JW (2009) White-rot basidiomycete-mediated decomposition of C60 fullerol. Environ Sci Technol 43:3162–3168. doi: 10.1021/es801873q CrossRefGoogle Scholar
  57. Simonin M, Richaume A (2015) Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environ Sci Pollut Res Int 22:13710–13723. doi: 10.1007/s11356-015-4171-x CrossRefGoogle Scholar
  58. Slavic M, Djordjevic A, Radojicic R, Milovanovic S, Orescanin-Dusic Z, Rakocevic Z, Spasic MB, Blagojevic D (2013) Fullerenol C60(OH)24 nanoparticles decrease relaxing effects of dimethyl sulfoxide on rat uterus spontaneous contraction. J Nanopart Res 15:1650. doi: 10.1007/s11051-013-1650-1 CrossRefGoogle Scholar
  59. Sporty JL, Kabir M, Turteltaub KW, Ognibene T, Bench G (2008) J Sep Sci 31:3202–3211. doi: 10.1002/jssc.200800238.Single CrossRefGoogle Scholar
  60. Stankov K, Borisev I, Kojic V, Rutonjski L, Bogdanovic G, Djordjevic A (2013) Modification of antioxidative and antiapoptotic genes expression in irradiated K562 cells upon fullerenol C60(OH)24 nanoparticle treatment. J Nanosci Nanotechnol 13:105–113. doi: 10.1166/jnn.2012.6847 CrossRefGoogle Scholar
  61. Unković N, Ljaljević Grbić M, Stupar M, Vukojević J, Janković V, Jović D, Đorđević A (2015) Aspergilli response to benzalkonium chloride and novel-synthesized fullerenol/benzalkonium chloride nanocomposite. Sci World J 2015:109262. doi: 10.1155/2015/109262 Google Scholar
  62. Yu J (2012) Current understanding on aflatoxin biosynthesis and future perspective in reducing aflatoxin contamination. Toxins (Basel) 4:1024–1057. doi: 10.3390/toxins4111024 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Tihomir Kovač
    • 1
    Email author
  • Bojan Šarkanj
    • 1
  • Tomislav Klapec
    • 1
  • Ivana Borišev
    • 2
  • Marija Kovač
    • 3
  • Ante Nevistić
    • 3
  • Ivica Strelec
    • 1
  1. 1.Faculty of Food Technology, Department of Applied Chemistry and EcologyJosip Juraj Strossmayer University of OsijekOsijekCroatia
  2. 2.Department of Chemistry, Biochemistry and Environmental protection, Faculty of SciencesUniversity of Novi SadNovi SadSerbia
  3. 3.Inspecto d.o.oĐakovoCroatia

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