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ORIGINAL ARTICLE
Physiological and Antagonistic Properties of Pichia kluyveri for Curative and Preventive Treatments Against Post-Harvest Fruit Fungi
 
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1
Post-Harvest and Agro-Processing Technologies, ARC Infruitec-Nietvoorbij (The Fruit, Vine and Wine Institute), Agricultural Research Council, South Africa
 
2
Bioresource Engineering Research Group (BioERG), Department of Biotechnology, Cape Peninsula University of Technology, South Africa
 
3
Center of Excellence in Carbon-Based Fuels, School of Chemical and Minerals Engineering, North-West University, Private Bag X1290, Potchefstroom 2520, South Africa
 
 
Submission date: 2021-05-04
 
 
Final revision date: 2021-06-18
 
 
Acceptance date: 2021-06-23
 
 
Online publication date: 2021-07-20
 
 
Publication date: 2021-07-20
 
 
Corresponding author
Heinrich Wilbur Du Plessis   

Bioresource Engineering Research Group (BioERG), Department of Biotechnology, Cape Peninsula University of Technology, P.O. Box 652, 8000, Cape Town, South Africa
 
 
Pol. J. Food Nutr. Sci. 2021;71(3):245-253
 
KEYWORDS
TOPICS
ABSTRACT
Postharvest fruit loss due to spoilage is mainly attributed to fungal infections. Synthetic chemicals can be used to preserve fruits, but they are expensive and pose risks to human health. The replacement of these chemicals by safer and cost- effective biocontrol agents is now a priority. This study investigated the physiological characteristics of Pichia kluyveri and its potential use as a biofungicide. The antagonistic effect of P. kluyveri against Botrytis cinerea and Monilinia laxa was tested on yeast peptone dextrose agar, grapes, apples, and pears. Yeast growth was variably possible at different temperatures, pH, and salinity levels. Strain-dependent antagonistic responses were observed on agar plates, where M. laxa was the more sensitive fungus to the antagonistic yeast. P. kluyveri demonstrated strong physiological properties under stressful temperature, pH, and salinity conditions. Preventive applications of P. kluyveri to apples were 95% effective against B. cinerea and 100% effective against M. laxa. Fruit type-dependent responses were evident on pears. Similarly, preventive application on grapes was also effective against the fungal pathogens studied. In general, the antagonistic responses were both fungus- and treatment- (curative and preventive) dependent. Therefore, the preventive use of P. kluyveri against post-harvest fruit-fungal infections proved to be an effective method for biological control of grapes, apples, and pears against fungal spoilage organisms Botrytis cinerea and Monilinia laxa.
FUNDING
This work was supported by the Agricultural Research Council (ARC) and National Research Foundation (NRF) of South Africa (Grant Numbers: SFP160505164079 and 117833). The opinions, findings and conclusions or recommendations expressed in this publication is that of the authors alone, and the NRF accepts no liability whatsoever in this regard. The authors thank the students, interns, technicians and research assistants who contributed.
 
REFERENCES (46)
1.
Aloui, H., Licciardello, F., Khwaldia, K., Hamdi, M., Restuccia, C. (2015). Physical properties and antifungal activity of bioactive films containing Wickerhamomyces anomalus killer yeast and their application for preservation of oranges and control of post-harvest green mold caused by Penicillium digitatum. International Journal of Food Microbiology, 200, 22–30. https://doi.org/10.1016/j.ijfo....
 
2.
Andrade, M.J., Thorsen, L., Rodríguez, A., Córdoba, J.J., Jespersen, L. (2014). Inhibition of ochratoxigenic moulds by Debaryomyces hansenii strains for biopreservation of dry-cured meat products. International Journal of Food Microbiology, 170, 70–77. https://doi.org/10.1016/j.ijfo....
 
3.
Benito, S., Palomero, F., Morata, A., Uthurry, C., Suárez-Lepe, J.A. (2009). Minimization of ethylphenol precursors in red wines via the formation of pyranoanthocyanins by selected yeasts. International Journal of Food Microbiology, 132(2-3), 145–152. https://doi.org/10.1016/j.ijfo....
 
4.
Buzzini, P., Martini, A. (2002). Extracellular enzymatic activity profiles in yeast and yeast-like strains isolated from tropical environments. Journal of Applied Microbiology, 93(2), 1020-1025. https://doi.org/10.1046/j.1365....
 
5.
Cape Farm Mapper. [http://gis.elsenburg.com/apps/...] (accessed: 6 June 2018).
 
6.
Çelik, Z.D., Erten, H, Darici, M., Cabaroğlu, T. (2017). Molecular characterization and technological properties of wine yeasts isolated during spontaneous fermentation of Vitis vinifera L. cv. Narince grape must grown in ancient wine making area Tokat, Anatolia. BIO Web of Conference, 9, art. no. 02017 https://doi.org/10.1051/biocon....
 
7.
Ciani, M., Fatichenti, F. (2001). Killer toxin of Kluyveromyces phaffii DBVPG 6076 as a biopreservative agent to control apiculate wine yeasts. Applied Environmental Microbiology, 67(7), 3058–3063. https://doi.org/10.1128/AEM.67....
 
8.
Comitini, F., De, J.I., Pepe, L., Mannazzu, I., Ciani, M. (2004a). Pichia anomala and Kluyveromyces wickerhamii killer toxins as new tools against Dekkera/Brettanomyces spoilage yeasts. FEMS Microbiology Letters, 238(1), 235–240. https://doi.org/10.1111/j.1574....
 
9.
Comitini, F., Di Pietro, N., Zacchi, L., Mannazzu, I., Ciani, M. (2004b). Kluyveromyces phaffii killer toxin active against wine spoilage yeasts: purification and characterization. Microbiology, 150(8), 2535–2541. https://doi.org/10.1099/mic.0.....
 
10.
Cordero-Bueso, G., Mangieri, N., Maghradze, D., Foschino, R., Valdetara, F., Cantoral, J.M., Vigentini, I. (2017). Wild grape-associated yeasts as promising biocontrol agents against Vitis vinifera fungal pathogens. Frontiers in Microbiology, 8, art. no. 2025. https://doi.org/10.3389/fmicb.....
 
11.
Crafack, M., Mikkelsen, M.B., Saerens, S., Knudsen, M., Blennow, A., Lowor, S., Takrama, J., Swiegers, J.H., Petersen, G.B., Heimdal, H. (2013). Influencing cocoa flavour using Pichia kluyveri and Kluyveromyces marxianus in a defined mixed starter culture for cocoa fermentation. International Journal of Food Microbiology, 167(1), 103–116. https://doi.org/10.1016/j.ijfo....
 
12.
Droby, S. (2005). Improving quality and safety of fresh fruits and vegetables after harvest by the use of biocontrol agents and natural materials. Acta Horticulturae, 709, 45–52. https://doi.org/10.17660/ActaH....
 
13.
Du Toit, M., Pretorius, I.S. (2000). Microbial spoilage and preservation of wine: using weapons from nature’s own arsenal – a review. South African Journal of Enology and Viticulture, 21(1), 74–96. https://doi.org/10.21548/21-1-....
 
14.
El-Ghaouth, A., Wilson, C., Wisniewski, M. (2004). Biologically-based alternatives to synthetic fungicides for the control of postharvest diseases of fruit and vegetables. In: Naqvi, S.A.M.H. (Eds.), Diseases of Fruits and Vegetables. Volume II. Springer, Dordrecht, pp. 511-535. https://doi.org/10.1007/1-4020....
 
15.
Fiori, S., Urgeghe, P.P., Hammami, W., Razzu, S., Jaoua, S., Migheli, Q. (2014). Biocontrol activity of four non-and low-fermenting yeast strains against Aspergillus carbonarius and their ability to remove ochratoxin A from grape juice. International Journal of Food Microbiology, 189, 45–50. https://doi.org/10.1016/j.ijfo....
 
16.
Fourie, P.H., Holz, G., Calitz, F.J. (2002). Occurrence of Botrytis cinerea and Monilinia laxa on nectarine and plum in Western Cape orchards, South Africa. Australasian Plant Pathology, 31, 197-204. https://doi.org/10.1071/AP0200....
 
17.
Fredlund, E., Blank, L.M., Schnürer, J., Sauer, U., Passoth, V. (2004). Oxygen-and glucose-dependent regulation of central carbon metabolism in Pichia anomala. Journal of Applied Environmental Microbiology, 70(10), 5905–5911. https://doi.org/10.1128/AEM.70....
 
18.
Gril, T., Celar, F., Munda, A., Javornik, B., Jakse, J. (2008). AFLP analysis of intraspecific variation between Monilinia laxa isolates from different hosts. Plant Disease, 92(12), 1616–1624. https://doi.org/10.1094/PDIS-9....
 
19.
Grzegorczyk, M., Żarowska, B., Restuccia, C., Cirvilleri, G. (2017). Post-harvest biocontrol ability of killer yeasts against Monilinia fructigena and Monilinia fructicola on stone fruit. Food Microbiology, 61, 93–101. https://doi.org/10.1016/j.fm.2....
 
20.
Hernández, A., Martín, A., Córdoba, M.G., Benito, M.J., Aranda, E., Pérez-Nevado, F. (2008). Determination of killer activity in yeasts isolated from the elaboration of seasoned green table olives. International Journal of Food Microbiology, 121(2), 178–188. https://doi.org/10.1016/j.ijfo....
 
21.
Huang, R., Che, H.J., Zhang, J., Yang, L., Jiang, D.H., Li, G.Q. (2012). Evaluation of Sporidiobolus pararoseus strain YCXT3 as biocontrol agent of Botrytis cinerea on post-harvest strawberry fruits. Biological Control, 62(1), 53–63. https://doi.org/10.1016/j.bioc....
 
22.
Huang, R., Li, G.Q., Zhang, J., Yang, L., Che, H.J., Jiang, D.H., Huang, H.C. (2011). Control of post-harvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology, 101(7), 859–869. https://doi.org/10.1094/PHYTO-....
 
23.
Jolly, N.P., Varela, C., Pretorius, I.S. (2014). Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Research, 14(2), 215-237. https://doi.org/10.1111/1567-1....
 
24.
Liu, J., Sui, Y., Wisniewski, M., Droby, S., Liu, Y. (2013). Review: utilization of antagonistic yeasts to manage post-harvest fungal diseases of fruit. International Journal of Food Microbiology, 167(2), 153–160. https://doi.org/10.1016/j.ijfo....
 
25.
Lutz, M.C., Lopes, C.A., Rodriguez, M.E., Sosa, M.C., Sangorrín, M.P. (2013). Efficacy and putative mode of action of native and commercial antagonistic yeasts against post-harvest pathogens of pear. International Journal of Food Microbiology, 164(2-3), 166–172. https://doi.org/10.1016/j.ijfo....
 
26.
Medina-Córdova, N., López-Aguilar, R., Ascencio, F., Castellanos, T., Campa-Córdova, A.I., Angulo, C. (2016). Biocontrol activity of the marine yeast Debaryomyces hansenii against phytopathogenic fungi and its ability to inhibit mycotoxins production in maize grain (Zea mays L.). Biological Control, 97, 70–79. https://doi.org/10.1016/j.bioc....
 
27.
Mehlomakulu, N.N., Setati, M.E., Divol, B. (2014). Characterization of novel killer toxins secreted by wine-related non-Saccharomyces yeasts and their action on Brettanomyces spp. International Journal of Food Microbiology, 188, 83–91. https://doi.org/10.1016/j.ijfo....
 
28.
Mewa-Ngongang, M., du Plessis, H.W., Hutchinson, U.F., Mekuto, L., Ntwampe, S.K. (2017). Kinetic modelling and optimisation of antimicrobial compound production by Candida pyralidae KU736785 for control of Candida guilliermondii. Food Science and Technology International, 23(4), 358–370. https://doi.org/10.1177/108201....
 
29.
Mewa-Ngongang, M., du Plessis, H.W., Ntwampe, S.K., Chidi, B.S., Hutchinson, U.F., Mekuto, L., Jolly, N.P. (2019a). Grape pomace extracts as fermentation medium for the production of potential biopreservation compounds. Foods, 8(2), art. no. 51. https://doi.org/10.3390/foods8....
 
30.
Mewa-Ngongang, M., du Plessis, H.W., Ntwampe, S.K.O., Chidi, B.S., Hutchinson, U.F., Mekuto, L., Jolly, N.P. (2019b). The use of Candida pyralidae and Pichia kluyveri to control spoilage microorganisms of raw fruits used for beverage production. Foods 8(10), art. no. 454. https://doi.org/10.3390/foods8....
 
31.
Morales, H., Marín, S., Rovira, A., Ramos, A.J., Sanchis, V. (2007). Patulin accumulation in apples by Penicillium expansum during postharvest stages. Letters in Applied Microbiology, 44(1), 30–35. https://doi.org/10.1111/j.1472....
 
32.
Muccilli, S., Restuccia, C. (2015). Bioprotective role of yeasts. Microorganisms, 3(4), 588–611. https://doi.org/10.3390/microo....
 
33.
Nally, M.C., Pesce, V.M., Maturano, Y.P., Rodriguez-Assaf, L.A., Toro, M.E., Castellanos de Figueroa, L.I., Vazquez, F. (2015). Antifungal modes of action of Saccharomyces and other biocontrol yeasts against fungi isolated from sour and grey rots. International Journal of Food Microbiology, 204, 91–100. https://doi.org/10.1016/j.ijfo....
 
34.
Núñez, F., Lara, M.S., Peromingo, B., Delgado, J., Sánchez-Montero, L., Andrade, M.J. (2015). Selection and evaluation of Debaryomyces hansenii isolates as potential bioprotective agents against toxigenic penicillia in dry-fermented sausages. Food Microbiology, 46, 114–120. https://doi.org/10.1016/j.fm.2....
 
35.
Oro, L., Ciani, M., Comitini, F. (2014). Antimicrobial activity of Metschnikowia pulcherrima on wine yeasts. ‎Journal of Applied Microbiology, 116(5), 1209–1217. https://doi.org/10.1111/jam.12....
 
36.
Parveen, S., Wani, A.H., Bhat, M.Y., Koka, J.A., Wani, F.A. (2016). Management of post-harvest fungal rot of peach (Prunus persica) caused by Rhizopus stolonifer in Kashmir Valley, India. Plant Patholology and Quarantine, 6(1), 19–29. https://doi.org/10.5943/ppq/6/....
 
37.
Psani, M., Kotzekidou, P. (2006). Technological characteristics of yeast strains and their potential as starter adjuncts in Greek‐style black olive fermentation. World Journal of Microbiology and Biotechnology, 22, 1329–1336. https://doi.org/10.1007/s11274....
 
38.
Sáez, J.S., Lopes, C.A., Kirs, V.C., Sangorrín, M.P. (2010). Enhanced volatile phenols in wine fermented with Saccharomyces cerevisiae and spoiled with Pichia guilliermondii and Dekkera bruxellensis. Letters in Applied Microbiology, 51(2), 170–176. https://doi.org/10.1111/j.1472....
 
39.
Sansone, G.Y., Lambrese, V., Calvente, G., Fernández, D., Benuzzi, M., Sanz Ferramola, M. (2018). Evaluation of Rhodosporidium fluviale as biocontrol agent against Botrytis cinerea on apple fruit. Letters in Applied Microbiology, 66(5), 455–461. https://doi.org/10.1111/lam.12....
 
40.
Sharma, R.R., Singh, D., Singh, R. (2009). Biological control of post-harvest diseases of fruits and vegetables by microbial antagonists: A review. Biological Control, 50(3), 205–221. https://doi.org/10.1016/j.bioc....
 
41.
Singh, D., Sharma, R.R. (2007). Post-Harvest Diseases Of Fruit, Vegetables, And Their Management, first ed. Daya Publishing House, New Delhi, India.
 
42.
Thompson, R.S., Aveling, T.A.S., Blanco, P.R. (2013). A new semi-selective medium for Fusarium graminearum, F. proliferatum, F. subglutinans and F. verticillioides in maize seed. South African Journal of Botany, 84, 94–101. https://doi.org/10.1016/j.sajb....
 
43.
Tipper, D.J., Bostian, K.A. (1984). Double-stranded ribonucleic acid killer systems in yeasts. Microbiological Reviews, 48(2), 125-156. https://doi.org/10.1128/mr.48.....
 
44.
Williamson, B., Tudzynski, B., Tudzynski, P., Van Kan, J.A. (2007). Botrytis cinerea: the cause of grey mould disease. Molecular Plant Pathology, 8(5), 561–580. https://doi.org/10.1111/j.1364....
 
45.
Zhu, C., Shi, J., Jiang, C., Liu, Y. (2015). Inhibition of the growth and ochratoxin A production by Aspergillus carbonarius and Aspergillus ochraceus in vitro and in vivo through antagonistic yeasts. Food Control, 50, 125–132. https://doi.org/10.1016/j.food....
 
46.
Zhu, S.J. (2006). Non-chemical approaches to decay control in post-harvest fruit. In Advances in Postharvest Technologies for Horticultural Crops. Research Signpost, Trivandrum, India, ISBN, 8130801108, pp. 297–313.
 
 
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