Comparison of Antimicrobial Activity of Essential Oils and Plant Extracts with Recombinant Peptide in Controlling of Some Pathogens of Cultivated White Button Mushrooms

Document Type : Research Article

Authors

• Farajollah Shahriari ¹
• Abbas Tanhaeian ²
• Mahdi Akhlaghi ²
• Narges Nazifi ²

¹ Ferdowsi university of Mashhad

² ferdowsi

https://doi.org/10.22067/jhorts4.v32i4.72136

Abstract

Introduction: The most serious diseases of cultivated mushrooms are caused by Pseudomonas tolaasii and Trichoderma harzianum pathogens. A common method of pathogen control on farms worldwide is the application of various chemical pesticides. Many of these substances are unsafe for human and environment. The interest in discovering and developing natural antimicrobials has significantly increased due to consumer preferences for foods that are free of chemical residues. So, a major challenge for mushroom growers is to control diseases with alternative compounds such as essential oils and plant extracts. Antimicrobial peptides (AMPs) were also known as potential antibiotic and considered as a new antimicrobial agents. In the present study, the antibacterial and antifungal potential of essential oils, plant extracts and a recombinant peptide were investigated for their pathogenicity. For this purpose, the essential oils of Cuminum cyminum and Zataria multiflora and the plant extracts of Dorema ammoniacum and Ferulago angulata and a recombinant peptide were evaluated for their antimicrobial and antifungal effects on the P. tolaasii and T. harzianum pathogens.
Materials and Methods: In this study, essential oils of C. cyminum and Z. multiflora were extracted by hydrodistillation in a Clevenger-type apparatus. The plant extracts (D. ammoniacum and F. angulata) were prepared using maceration method. Recombinant peptides (Lactoferricin-Lactoferrampin) were produced from Adherent Human Embryonic Kidney 293 (HEK293). The antifungal properties of essential oils, plant extract and AMPs were studied on growth inhibition. Antibacterial activity of substances were tested against P. tolaasii via disk-diffusion method respectively. Minimum inhibitory concentration (MIC), Minimum bactericidal concentration (MBC) and Minimum fungicidal concentration (MFC) to the compounds were studied. All treatments were considered in a completely randomized block design with three replicates.
Results: The results of the antibacterial evaluations showed that the Chimera peptide have remarkable activity  against pathogenic bacteria with a mean diameter of the zone inhibition region of 32.2mm, followed by C. cyminum and D. ammoniacum extracts with mean values of 7 and 6 mm respectively. Regarding to antifungal activity of substances isolated from above material, it was found that essential oils of C. cyminum and Z. multiflora completely prevent the growth of T. harzianum, followed by D. ammoniacum and F. angulate with maen values of 26 and 60.6 mm respectively. The lowest antifungal activity was observed for chimera peptide.
Discussion: The cultivated button mushroom is one of the most extensively cultivated mushroom in the world. The most serious diseases of cultivated mushrooms are caused by P. tolaasii and T. harzianum pathogens. The results of our study showed that the C. cyminum and D. ammoniacum have remarkable activity against pathogenic bacteria. Plant extracts, essential oils and their components have demonstrated strong fungistatic and antibacterial effects against pathogenic fungi and bacteria on cultivated mushrooms. Modes of action of essential oils in their interaction with bacteria have been quite revealed. It has been assumed that Thymol changes the permeability of cytoplasmic membrane of Gram-positive bacteria, acting as a proton exchanger, decreasing the pH gradient and causing a collapse of the proton motive force and eventually cell death. Regarding to antifungal activity, our results also showed that essential oils of C. cyminum and Z. multiflora completely prevent the growth of T. harzianum, followed by D. ammoniacum and F. angulate. One of the possible action mechanisms proposed that fungal growth may be reduced or totally inhibited due to monoterpenes present in essential oils which could increase the concentration of lipidic peroxides such as hydroxyl, alkoxyl and alkoperoxyl radicals and so bring about cell death. According to another mechanism, the essential oils would act on the hyphae of the mycelium, provoking exit of components from the cytoplasm, the loss of rigidity and integrity of the hypha cell wall, resulting in its collapse and death of the mycelium. In our study, a camel recombinant chimeric lactoferricin + lactoferrampin peptide was also tested for its antimicrobial activity. Our result showed that this recombinant peptide have remarkable activity against pathogenic bacteria. The details of the antibacterial mechanism for this recombinant peptide still are unknown. However, amino acid profile, sequence orientation and structural conformation of cationic peptides are the main features which make these peptides capable to inhibit bacterial growth by disrupting of the bacterial cell membrane. As a general results it can be concluded that natural plant-derived antimicrobial as well as recombinant peptides can be used as alternatives to synthetic pesticides, however, further studies on safety and toxicity of these substances should be carried out before use.
Conclusion: In summary, this study shows that essential oils and plant extracts isolated from above plant material have remarkable antifungal activities against T. harzianum, while the chimera peptide showed complete inhibition against P. tolaasii. Thus all of these substance could become alternative to synthetic antimicrobial compounds for control of mushroom pathogens. However, further studies on safety and toxicity of these substances should be carried out before use.

Keywords

• antimicrobial
• Chimeric peptide
• Essential oils
• Plant extract
• White button mushrooms

20.1001.1.20084730.1397.32.4.11.6

References

1- Ali G.S., and Reddy A. 2000. Inhibition of fungal and bacterial plant pathogens by synthetic peptides: in vitro growth inhibition, interaction between peptides and inhibition of disease progression. Molecular Plant-microbe Interactions, 13(8): 847-859.

2- Akhlaghi M., Tarighi S., Farsi M., and Taheri P. 2015. Identification and investigation of some virulence factors of Pseudomonas tolaasii isolated from mushroom in Iran. Iranian Journal of Plant Pathology, 51(4): 399-412. (In Persian)

3- Akhlaghi M., Tanhaiyan A., Shahriari F., and Tarighi S. 2016. Evaluating the Antibacterial Effect of the Lactoferrin-lactoferricin Chimeric Protein Obtained from the Domestic Livestock’s Milk on Pathogenic Bactria of Pseudomonas tolaasii. Proceedings of 22nd Iranian Plant Protection Congress, 27- 30 August, 2016. (In Persian with English abstract)

4- Amini J., Farhang V., Javadi T., and Nazemi J. 2016. Antifungal effect of plant essential oils on controlling Phytophthora species. Plant Pathology Journal, 32(1): 16. (In Persian with English abstract)

5- Andersson H., Tago D., and Treich N. 2014. Pesticides and health: A review of evidence on health effects, valuation of risks, and benefit‐cost analysis. Preference Measurement in Health, 1-61.

6- Azizi Bargini K. 2013. Evaluation of antimicrobial activity of Cecropin-Melittin Cimmer peptide alone and with common antibiotics against common bacterial infections in hospitals. MC thesis degree, University of Mohaghegh Ardabili, 2013.

7- Bradshaw J.P. 2003. Cationic antimicrobial peptides. Bio Drugs, 17(4): 233-240.

8- Bruni N., Capucchio M.T., Biasibetti E., Pessione E., Cirrincione S., Giraudo L., Corona A., and Dosio F. 2016 Antimicrobial activity of Lactoferrin-related peptides and applications in human and veterinary medicine. Molecules 21(6): 752.

9- Clinical and Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Test for Bacteria that Grow Aerobically: Approved Standard 8th Edition; CLSI Document M07-A8; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2009.

10- Charles D.J., and Simon J.E. 1990. Comparison of extraction methods for the rapid determination of essential oil content and composition of basil. Journal of the American Society for Horticultural Science, 115: 458-462.

11- Damalas C.A., and Eleftherohorinos I.G. 2011. Pesticide exposure, safety issues, and risk assessment indicators. International Journal of Environmental Research and Public Health, 8(5): 1402-1419.

12- Datta A., Bhattacharyya D., Singh S., Ghosh A., Schmidtchen A., and Malmsten M. 2016. Role of aromatic amino acids in lipopolysaccharide and membrane interactions of antimicrobial peptides for use in plant disease control. Journal of Biological Chemistry, 291(25): 13301-17.

13- Dayan F.E., Cantrell C.L., and Duke S.O. 2009. Natural products in crop protection. Bioorganic and Medicinal Chemistry, 17(12): 4022-34.

14- Dehghan G.R., Zarini G.R., and Hajizadeh M. 2013. Phytochemical investigation and antimicrobial, antifungal and synergistic activities of chloroform fractions of the root of Ferula szovitsiana. Journal of Shahrekord University of Medical Sciences, 15(6): 10-17. (In Persian with English abstract)

15- Embleton N.D., Berrington J.E., McGuire W., Stewart C.J., and Cummings S.P. 2013. Lactoferrin: Antimicrobial activity and therapeutic potential. Seminars in Fetal and Neonatal Medicine, 18(3): 143-9.

16- Eslahi N., Niazi A., Aram F., Afsharifar A., and Taghavi S.M. 2015. Overexpression of Camel lactoferricin recombinant peptide in tobacco hairy roots and study of its antimicrobial activity. Iranian Journal of Plant Pathology, 51(4): 431-444.

17- Farag R., Daw Z., Hewedi F., and El-Baroty G. 1989. Antimicrobial activity of some Egyptian spice essential oils. Journal of Food Protection, 52(9): 665-7.

18- Fayaz F., Rahmati Roodsari S., Gachkar L., Pourkaveh B., and Ghasemian Safaei H. 2016. The Antimicrobial activity of Ferula gummosa on bacterial strains isolated from patients with gastroenteritis. Iranian Journal of Clinical Infectious Diseases, 6: 20-4. (In Persian with English abstract)

19- Fukuta S., Kawamoto K.I., Mizukami Y., Yoshimura Y., Ueda J.I., and Kanbe M. 2012. Transgenic tobacco plants expressing antimicrobial peptide bovine lactoferricin show enhanced resistance to phytopathogens. Plant Biotechnology, 29: 383-389.

20- Garcia-Montoya I.A., Cendon T.S., Arevalo-Gallegos S., and Rascon-Cruz Q. 2012. Lactoferrin a multiple bioactive protein: an overview. Biochemical et Biophysical Acta (BBA)-General Subjects, 1820(3): 226-36.

21- Gea F.J., Navarro M.J., and Tello J.C. 2005. Reduced sensitivity of the mushroom pathogen Verticillium fungicola to prochloraz-manganese in vitro. Mycological Research, 109(6): 741-5.

22- Gurjar M.S., Ali S., Akhtar M., and Singh K.S. 2012. Efficacy of plant extracts in plant disease management. Agricultural Science, 3(3): 425.

23- Hamidi M., Mousavi Nasab S.D., Ahmadi N., Basati G.h., Aolad G.R., Salimian J., and Zargar M. 2013. Synthesis of antimicrobial peptides in bacteria. Scientific Journal of Ilam University of Medical Sciences, 20(4).

24- Hassani A., Jalili Marndi R., and Qusta Y. 2010. Use of essential oils for controlling mildew (Botrytis cinerea) disease Pear fruit. Iranian Journal of Horticultural Science, 40-1(85-94). (In Persian with English abstract)

25- Iacobellis N.S., Lo Cantore P., Capasso F., and Senatore F. 2005. Antibacterial activity of Cuminum cyminum L. and Carum carvi L. essential oils. Journal of Agricultural and Food Chemistry, 53(1): 57-61.

26- Iglesias-Figueroa B., Valdiviezo-Godina N., Siqueiros-Cendon T., Sinagawa-Garcia S., Arevalo-Gallegos S., and Rascon-Cruz Q. 2016. High-level expression of recombinant bovine lactoferrin in Pichia pastoris with antimicrobial activity. International Journal of Molecular Sciences, 17(6): 902.

27- Kakon A., Choudhury M.B.K., and Saha S. 2012. Mushroom is an ideal food supplement. Journal of Dhaka National Medical College & Hospital, 18(1): 58-62.

28- Kumar R., Saha A., and Saha D. 2012. A new antifungal coumarin from Clausena excavata Fitoterapia, 83(1):

230-3.

29- Li Y. 2011. Recombinant production of antimicrobial peptides in Escherichia coli: a review. Protein Expression and Purification, 80(2): 260-7.

30- Lopez P., Sanchez C., Batlle R., and Nerin C. 2005 . Solid-and vapor-phase antimicrobial activities of six essential oils: susceptibility of selected foodborne bacterial and fungal strains. Journal of Agricultural and Food Chemistry, 53(17): 6939-46.

31- Mattila P., Suonpä K., and Piironen V. 2000. Functional properties of edible mushrooms. Nutrition, 16(7–8): 694–6.

32- Mzida M., Ben Khedira S., Ben Salemb M., Regaiegb W., and Rebaia T. 2016. Antioxidant and antimicrobial activities of ethanol and aqueous extracts from Urtica urens. Pharmaceutical Biology, 55(1): 775–781.

33- Mosch J., Zeller W., Rieck M., Ullrich W., and Bonn W.G. Further studies on plant extracts with a resistance induction effect against Erwinia amylovora. International workshop on fire blight, Acta hort, 411: 361 - 6.

34- Plodpai P., Chuenchitt S., Petcharat V., Chakthong S., and Voravuthikunchai S.P. 2013. Anti-Rhizoctonia solani activity by Desmos chinensis extracts and its mechanism of action. Crop Prot. 43: 65–71.

35- Potočnik I., Vukojević J., Stajić M., Rekanović E., Milijašević S., and Stepanović M. 2009. Toxicity of fungicides with different modes of action to Cladobotryum dendroides and Agaricus bisporus. Journal of Environmental Science and Health Part B., 44(8): 823-7.

36- Sadeghi M., and Hojati Z. 2016. Evaluation of anticancer peptide VEGF111b secretion in HEK293 human Cells. Feyz Journal of Kashan University of Medical Sciences, 21(1): 28-34

37- Sadler M. 2003. Nutritional properties of edible fungi. Nutrition Bulletin, 28(3): 305-308.

38- Samuelsen A.B. 2007. The traditional uses, chemical constituents and biological activities of Plantago major L. A review. Journal of Ethnopharmacology, 71(1): 1-21.

39- Singh G., Kapoor I., Pandey S., Singh U., and Singh R. 2002. Studies on essential oils: part 10; antibacterial activity of volatile oils of some spices. Phytotherapy Research, 16(7): 680-2.

40- Sinha M., Kaushik S., Kaur P., Sharma S., and Singh T.P. 2013. Antimicrobial Lactoferrin peptides: The hidden players in the protective function of a multifunctional protein. International Journal of Peptides, 2013: 12.

41- Sokovic M., and Van Griensven L. 2006. Antimicrobial activity of essential oils and their components against the three major pathogens of the cultivated button mushroom, Agaricus bisporus. European Journal of Plant Pathology, 116: 211–224.

42- Wang W.Y., Wong J.H., Ip D.T.M., Wan D.C.C., Cheung R.C., and Ng T.B. 2016. Bovine Lactoferrampin, Human Lactoferricin, and Lactoferrin 1-11 Inhibit Nuclear Translocation of HIV Integrase. Applied Biochemistry and Biotechnology, 179(7): 1202-12.