Advertisement

Food Biophysics

, Volume 14, Issue 1, pp 97–107 | Cite as

Antifungal Actions of Glycinin Basic Peptide against Aspergillus niger through the Collaborative Damage to Cell Membrane and Mitochondria

  • Linhui Feng
  • Yingqiu LiEmail author
  • Zhaosheng Wang
  • Lianqing Qi
  • Haizhen Mo
ORIGINAL ARTICLE
  • 59 Downloads

Abstract

The objective of this work was to investigate antifungal actions of glycinin basic peptide (GBP), a natural preservative derived from soybean, against Aspergillus niger (A. niger). GBP exhibited the antifungal activity against A. niger with minimum inhibitory concentration of 1.5 mg/mL. The analysis of FSC and SSC manifested that GBP treatment could cause A. niger cells to shrink to become small and their granularity to complicate. And observations of electron microscopy directly showed more than 1.5 mg/mL GBP obviously destructed membrane, morphology, and organelles of mycelia and spores. The K+, Ca2+, and Mg2+ leakage further verified the disruptive region of GBP was membrane of A. niger. Moreover, the mitochondrial dysfunction by GBP was elucidated by the increase of intracellular reactive oxygen species and decrease of mitochondrial membrane potential. Taken together, GBP induced cellular damage and death of A. niger by collaborative action on cell membrane and mitochondria.

Keywords

Glycinin basic peptide Aspergillus niger Antifungal actions Cell membrane Mitochondria 

Notes

Acknowledgements

The authors would like to express their gratitude to the National Natural Science Foundation of China (31371839), Major Plan of Studying and Developing (2018YYSP001), 2017-year Support Program for Introduction of Urgently-needed talents in Western Economic Upwarping Zone and Poverty-alleviation-exploitation Key Area in Shandong Province, as well as the Program for Science and Technology Innovation Team in Universities of Henan Province (16IRTSTHN007).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    A. Sokmen, M. Gulluce, H.A. Akpulat, D. Daferera, B. Tepe, M. Polissiou, M. Sokmen, F. Sahin, The in vitro antimicrobial and antioxidant activities of the essential oils and methanol extracts of endemic Thymus spathulifolius. Food Control 15(8), 627–634 (2004)CrossRefGoogle Scholar
  2. 2.
    V.C.H. Wu, X.J. Qiu, B.G. de los Reyes, C.S. Lin, Y.P. Pan, Application of cranberry concentrate (Vaccinium macrocarpon) to control Escherichia coli O157:H7 in ground beef and its antimicrobial mechanism related to the downregulated slp, hdeA and cfa. Food Microbiol. 26(1), 32–38 (2009)CrossRefGoogle Scholar
  3. 3.
    S. Marín, M.E. Guynot, V. Sanchis, J. Arbonés, A.J. Ramos, Aspergillus flavus, Aspergillus niger, and Penicillium corylophilum spoilage prevention of bakery products by means of weak-acid preservatives. J. Food Sci. 67(6), 2271–2277 (2002)CrossRefGoogle Scholar
  4. 4.
    G.F. Mehyar, H.M. Al-Qadiri, H.A. Abu-Blan, B.G. Swanson, Antifungal effectiveness of potassium sorbate incorporated in edible coatings against spoilage molds of apples, cucumbers, and tomatoes during refrigerated storage. J. Food Sci. 76(3), M210–M217 (2011)CrossRefGoogle Scholar
  5. 5.
    S.C. Park, J.Y. Kim, J.K. Lee, I. Hwang, H. Cheong, J.W. Nah, K.S. Hahm, Y. Park, Antifungal mechanism of a novel antifungal protein from pumpkin rinds against various fungal pathogens. J. Agric. Food Chem. 57(19), 9299–9304 (2009)CrossRefGoogle Scholar
  6. 6.
    H.J. Kim, H.J. Suh, C.H. Lee, J.H. Kim, S.C. Kang, S. Park, J.S. Kim, Antifungal activity of glyceollins isolated from soybean elicited with Aspergillus sojae. J. Agric. Food Chem. 58(17), 9483–9487 (2010)CrossRefGoogle Scholar
  7. 7.
    Y.Q. Li, Q. Han, J.L. Feng, W.L. Tian, H.Z. Mo, Antibacterial characteristics and mechanisms of ɛ-poly-lysine against Escherichia coli and Staphylococcus aureus. Food Control 43, 2507–2515 (2014)Google Scholar
  8. 8.
    L. Zhang, A. Rozek, R.E.W. Hancock, Interaction of cationic antimicrobial peptides with model membranes. J. Biol. Chem. 276(38), 35714–35722 (2001)CrossRefGoogle Scholar
  9. 9.
    S. Damodaran, J.E. Kinsella, Effect of conglycinin on the thermal aggregation of glycinin. J. Agric. Food Chem. 30(5), 812–817 (1982)CrossRefGoogle Scholar
  10. 10.
    S. Hu, H. Liu, S. Qiao, P. He, X. Ma, W. Lu, Development of immunoaffinity chromatographic method for isolating glycinin (11S) from soybean proteins. J. Agric. Food Chem. 61(18), 4406–4410 (2013)CrossRefGoogle Scholar
  11. 11.
    M.Z. Sitohy, S.A. Mahgoub, A.O. Osman, In vitro and in situ antimicrobial action and mechanism of glycinin and its basic subunit. Int. J. Food Microbiol. 154(1), 19–29 (2012)CrossRefGoogle Scholar
  12. 12.
    Y.Q. Li, X.X. Sun, J.L. Feng, H.Z. Mo, Antibacterial activities and membrane permeability actions of glycinin basic peptide against Escherichia coli. Innovative Food Sci. Emerg. Technol. 31, 170–176 (2014)CrossRefGoogle Scholar
  13. 13.
    J. Yang, G.J. Sun, Y.Q. Li, K.Y. Cui, H.Z. Mo, Antibacterial characteristics of glycinin basic polypeptide against Staphylococcus aureus. Food Sci. Biotechnol. 25(5), 1477–1483 (2016)CrossRefGoogle Scholar
  14. 14.
    J. Hou, Y.Q. Li, Z.S. Wang, G.J. Sun, H.Z. Mo, Applicative effect of glycinin basic polypeptide in fresh wet noodles and antifungal characteristics. LWT-food. Sci. Technol. 83, 267–274 (2017)Google Scholar
  15. 15.
    T. Nagano, M. Hirotsuka, H. Mori, K. Kohyama, K. Nishinari, Dynamic viscoelastic study on the gelation of 7S globulin from soybeans. J. Agric. Food Chem. 40(6), 941–944 (1992)CrossRefGoogle Scholar
  16. 16.
    G. Ruchi, S. Sheela, Antifungal effect of antimicrobial peptides (AMPs LR14) derived from Lactobacillus plantarum strain LR/14 and their applications in prevention of grain spoilage. Food Microbiol. 42, 1–7 (2014)CrossRefGoogle Scholar
  17. 17.
    Y.Z. Wang, X.B. Zeng, Z.K. Zhou, K. Xing, A. Tessemac, H. Zeng, J. Tiana, Inhibitory effect of nerol against Aspergillus niger on grapes through a membrane lesion mechanism. Food Control 55, 54–61 (2015)CrossRefGoogle Scholar
  18. 18.
    K.D. Choi, H.Y. Kim, I.S. Shin, Antifungal activity of isothiocyanates extracted from horseradish (Armoracia rusticana) root against pathogenic dermal fungi. Food Sci. Biotechnol. 26(3), 847–852 (2017)CrossRefGoogle Scholar
  19. 19.
    J. Tian, Y.Z. Wang, Z.Q. Lu, C.H. Sun, M. Zhang, A.H. Zhu, X. Peng, Perillaldehyde, a promising antifungal agent used in food preservation, triggers apoptosis through a metacaspase-dependent pathway in Aspergillus flavus. J. Agric. Food Chem. 64(39), 7404–7413 (2016)CrossRefGoogle Scholar
  20. 20.
    W.R. Li, Q.S. Shi, Y.S. Ouyang, Y.B. Chen, S.S. Duan, Antifungal effects of citronella oil against Aspergillus niger ATCC 16404. Appl. Microbiol. Biotechnol. 97(16), 7483–7492 (2013)CrossRefGoogle Scholar
  21. 21.
    S. Manso, F. Cacho-Nerin, R. Becerril, C. Nerín, Combined analytical and microbiological tools to study the effect on Aspergillus flavus of cinnamon essential oil contained in food packaging. Food Control 30(2), 370–378 (2013)CrossRefGoogle Scholar
  22. 22.
    A.S.Y. Ting, E. Jioe, In vitro assessment of antifungal activities of antagonistic fungi towards pathogenic Ganoderma boninense under metal stress. Biol. Control 96, 57–63 (2016)CrossRefGoogle Scholar
  23. 23.
    J. Tian, X.B. Zeng, Z.Z. Feng, X.M. Miao, X. Peng, Y.W. Wang, Zanthoxylum molle Rehd. Essential oil as a potential natural preservative in management of Aspergillus flavus. Ind. Crop. Prod. 60, 151–159 (2014)CrossRefGoogle Scholar
  24. 24.
    T. Wu, D. Cheng, M.Y. He, S.Y. Pan, X.L. Yao, X.Y. Xu, Antifungal action and inhibitory mechanism of polymethoxylated flavoned from Citrus reticulate Blanco peel against Aspergillus niger. Food Control 35(1), 354–359 (2014)CrossRefGoogle Scholar
  25. 25.
    J. Yun, D.G. Lee, Cecropin A-induced apoptosis is regulated by ion balance and glutathione antioxidant system in Candida albicans. IUBMB Life 68(8), 652–662 (2016)CrossRefGoogle Scholar
  26. 26.
    J. Tian, X.Q. Ban, H. Zeng, J.S. He, Y.X. Chen, Y.W. Wang, The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS One 7(1), e30147 (2012)CrossRefGoogle Scholar
  27. 27.
    L.R. Li, Y.H. Shi, M.J. Cheserek, G.F. Su, G.W. Le, Antibacterial activity and dual mechanisms of peptide analog derived from cell-penetrating peptide against Salmonella typhimurium and Streptococcus pyogenes. Appl. Microbiol. Biotechnol. 97(4), 1711–1723 (2013)CrossRefGoogle Scholar
  28. 28.
    H.J. Lee, J.S. Hwang, D.G. Lee, Scolopendin, an antimicrobial peptide from centipede, attenuates mitochondrial functions and triggers apoptosis in Candida albicans. Biochem. J. 474(5), 635–645 (2017)CrossRefGoogle Scholar
  29. 29.
    G.P. Zhao, Y.Q. Li, G.J. Sun, H.Z. Mo, Antibacterial actions of glycinin basic peptide against Escherichia coli. J. Agric. Food Chem. 65(25), 5173–5180 (2017)CrossRefGoogle Scholar
  30. 30.
    J. Zhang, X. Wu, S.Q. Zhang, Antifungal mechanism of antibacterial peptide, ABP-CM4, from Bombyx mori against Aspergillus niger. Biotechnol. Lett. 30(12), 2157–2163 (2008)CrossRefGoogle Scholar
  31. 31.
    S. Shabala, L. Shabala, Ion transport and osmotic adjustment in plants and bacteria. Biomol Concepts 2(5), 407–419 (2011)CrossRefGoogle Scholar
  32. 32.
    D.G. Lee, H.N. Kim, Y. Park, H.K. Kim, B.H. Choi, C.H. Choi, K.S. Hahm, Design of novel analogue peptides with potent antibiotic activity based on the antimicrobial peptide, HP (2–20), derived from N-terminus of Helicobacter pylori ribosomal protein L1. Biochim Biophys Acta, Proteins Proteomics. 1598, 185–194 (2002)CrossRefGoogle Scholar
  33. 33.
    L.R. Li, J. Sun, S.F. Xia, X. Tian, M. Cheserek, G.W. Le, Mechanism of antifungal activity of antimicrobial peptide APP, a cell-penetrating peptide derivative, against Candida albicans: Intracellular DNA binding and cell cycle arrest. Appl. Microbiol. Biotechnol. 100(7), 3245–3253 (2016)CrossRefGoogle Scholar
  34. 34.
    K. Akash, K.D. Abhishek, K.J. Dhruva, K.D. Nawal, Efficacy of Mentha spicata essential oil in suppression of Aspergillus flavus and aflatoxin contamination in chickpea with particular emphasis to mode of antifungal action. Protoplasma 253(3), 647–653 (2016)CrossRefGoogle Scholar
  35. 35.
    T. Wu, D. Cheng, M.Y. He, S.Y. Pan, X.L. Yao, X.Y. Xu, Antifungal action and inhibitory mechanism of polymethoxylated flavones from Citrus reticulata Blanco peel against Aspergillus niger. Food Control 35(1), 354–359 (2014)CrossRefGoogle Scholar
  36. 36.
    N. Delattin, B.P. Cammue, K. Thevissen, Reactive oxygen species-inducing antifungal agents and their activity against fungal biofilms. Future Med. Chem. 6(1), 77–90 (2014)CrossRefGoogle Scholar
  37. 37.
    M. Sharma, R. Manoharlal, N. Puri, R. Prasad, Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressor TUP1 in Candida albicans. Biosci. Rep. 30(6), 391–404 (2010)CrossRefGoogle Scholar
  38. 38.
    A. Lupetti, A.P. Annema, S. Senesi, M. Campa, J.T.V. Dissel, P.H. Nibbering, Internal thiols and reactive oxygen species in candidacidal activity exerted by an N-terminal peptide of human lactoferrin. Antimicrob. Agents Chemother. 46(6), 1634–1639 (2002)CrossRefGoogle Scholar
  39. 39.
    J.J. Cheng, T.S. Park, L.C. Chio, A.S. Fischl, X.S. Ye, Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans. Mol. Cell. Biol. 23(1), 163–177 (2003)CrossRefGoogle Scholar
  40. 40.
    A. Lachelle, R.R. Jason, L. Sebastian, W. Regine, N.T. Gregory, Membrane activity of biomimetic facially amphiphilic antibiotics. J. Phys. Chem. B 110(8), 3527–3532 (2006)CrossRefGoogle Scholar
  41. 41.
    M. Giudici, J.A. Poveda, M.L. Molina, L.D.L. Canal, R.J.M. González, K. Pfüller, U. Pfüller, J. Villalaín, Antifungal effects and mechanism of action of viscotoxin A3. FEBS J. 273(1), 72–83 (2006)CrossRefGoogle Scholar
  42. 42.
    L. Kaiserer, C. Oberparleiter, G.R. Weiler, W. Burgstaller, E. Leiter, F. Marx, Characterization of the Penicillium chrysogenum antifungal protein PAF. Arch. Microbiol. 180(3), 204–210 (2003)CrossRefGoogle Scholar
  43. 43.
    R. Petruzzelli, M.E. Clementi, S. Marini, M. Coletta, E.D. Stasio, B. Giardina, F. Misiti, Respiratory inhibition of isolated mammalian mitochondria by salivary antifungal peptide histatin-5. Biochem. Biophys. Res. Commun. 311(4), 1034–1040 (2003)CrossRefGoogle Scholar
  44. 44.
    U. Schönfelder, A. Radestock, P. Elsner, U.C. Hipler, Cyclodextrin-induced apoptosis in human keratinocytes is caspase-8 dependent and accompanied by mitochondrial cytochrome c release. Exp. Dermatol. 15(11), 883–890 (2006)CrossRefGoogle Scholar
  45. 45.
    M.T. Andrés, M.V. Díaz, J.F. Fierro, Human lactoferrin induces apoptosis-like cell death in Candida albicans: Critical role of K+-channel-mediated K+ efflux. Antimicrob. Agents Chemother. 52(11), 4081–4088 (2008)CrossRefGoogle Scholar
  46. 46.
    E.M. Barbu, F. Shirazi, D.M. Mcgrath, N. Albert, R.L. Sidman, R. Pasqualini, W. Arap, D.P. Kontoyiannis, An antimicrobial peptidomimetic induces Mucorales cell death through mitochondria-mediated apoptosis. PLoS One 8(10), e76981 (2013)CrossRefGoogle Scholar
  47. 47.
    J. Reiter, E. Herker, F. Madeo, M.J. Schmitt, Viral killer toxins induce caspase-mediated apoptosis in yeast. J. Cell Biol. 168(3), 353–358 (2005)CrossRefGoogle Scholar
  48. 48.
    J. Lee, J.S. Hwang, I.S. Hwang, J. Cho, E. Lee, Y. Kim, D.G. Lee, Coprisin-induced antifungal effects in Candida albicans correlate with apoptotic mechanisms. Free Radic. Biol. Med. 52(11-12), 2302–2311 (2012)CrossRefGoogle Scholar
  49. 49.
    J.H. Hwang, I.S. Hwang, Q.H. Liu, E.R. Woo, D.G. Lee, (+)-Medioresinol leads to intracellular ROS accumulation and mitochondria-mediated apoptotic cell death in Candida albicans. Biochimie 94(8), 1784–1793 (2012)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Linhui Feng
    • 1
  • Yingqiu Li
    • 1
    Email author
  • Zhaosheng Wang
    • 2
  • Lianqing Qi
    • 3
  • Haizhen Mo
    • 4
  1. 1.School of Food Science & EngineeringQilu University of Technology (Shandong Academy of Sciences)JinanChina
  2. 2.Key Laboratory of Food Processing Technology and Quality Control in Shandong Province, School of Food Science and EngineeringShandong Agricultural UniversityTaianChina
  3. 3.School of Shandong Radio and TV UniversityJinanChina
  4. 4.School of Food ScienceHenan Institute of Science and TechnologyXinxiangChina

Personalised recommendations