Killer Yeast, a Novel Biological Control of Soilborne Diseases for Good Agriculture Practice

  • Azzam Aladdin
  • Julián Rafael Dib
  • Roslinda Abd. Malek
  • Hesham A. El EnshasyEmail author
Part of the Applied Environmental Science and Engineering for a Sustainable Future book series (AESE)


Aspergillus niger (A. niger) causes a disease called black mold on certain fruits and vegetables such as grapes, apricots, onions, and peanuts and is a common contaminant of food. Containment of this disease can reduce the amount of fruits, vegetables, and foods to be discarded, hence reducing the amounts of agricultural waste generated. Chemical control of A. niger has been partially successful, and fungicides are commonly used in the management of black mold. However, the risk of the establishment of resistant Aspergillus strains is considerable. Biocontrol, a nonhazardous alternative to the use of chemical fungicides, involves the use of biological processes to reduce crop loss and various microorganisms. Since it was first reported, the killer phenomenon in yeasts has been extensively studied in several genera and species, and its importance is gaining further recognition by industrialists. The food and beverage industries were among the first to explore the ability of toxin-producing yeasts to kill other fungus.


Killer yeast Biological control Good agriculture practice Soilborne disease 


  1. Abbasi P, Al-Dahmani J, Sahin F, Hoitink H, Miller S (2002) Effect of compost amendments on disease severity and yield of tomato in conventional and organic production systems. Plant Dis 86(2):156–161CrossRefGoogle Scholar
  2. Abd-Elgawad M, El-Mougy N, El-Gamal N, Abdel-Kader M, Mohamed M (2010) Protective treatments against soilborne pathogens in citrus orchards. J Plant Protect Res 50(4):477–484CrossRefGoogle Scholar
  3. Akhtar M, Malik A (2000) Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour Technol 74(1):35–47CrossRefGoogle Scholar
  4. Aldanondo AM, Almansa C (2009) The private provision of public environment: consumer preferences for organic production systems. Land Use Policy 26(3):669–682CrossRefGoogle Scholar
  5. Al-Naemi FA, Ahmed TA, Nishad R, Radwan O (2016) Antagonistic effects of Trichoderma harzianum isolates against Ceratocystis radicicola: pioneering a biocontrol strategy against black scorch disease in date palm trees. J Phytopathol 164(7–8):433–570Google Scholar
  6. Alonso LM, Kleiner D, Ortega E (2008) Spores of the mycorrhizal fungus Glomus mosseae host yeasts that solubilize phosphate and accumulate polyphosphates. Mycorrhiza 18(4):197–204CrossRefGoogle Scholar
  7. Amani H, Mehrnia MR, Sarrafzadeh MH, Haghighi M, Soudi MR (2010) Scale up and application of biosurfactant from Bacillus subtilis in enhanced oil recovery. Appl Biochem Biotechnol 162(2):510–523CrossRefGoogle Scholar
  8. Amprayn KO, Rose MT, Kecskés M, Pereg L, Nguyen HT, Kennedy IR (2012) Plant growth promoting characteristics of soil yeast (Candida tropicalis HY) and its effectiveness for promoting rice growth. Appl Soil Ecol 61:295–299CrossRefGoogle Scholar
  9. Arras G, Cicco VD, Arru S, Lima G (1998) Biocontrol by yeasts of blue mould of citrus fruits and the mode of action of an isolate of Pichia guilliermondii. J Hortic Sci Biotechnol 73(3):413–418CrossRefGoogle Scholar
  10. Aryantha I, Cross R, Guest D (2000) Suppression of Phytophthora cinnamomi in potting mixes amended with uncomposted and composted animal manures. Phytopathology 90(7):775–782CrossRefGoogle Scholar
  11. Awad HM, El-Enshasy HA, Hanapi SZ, Hamed ER, Rosidi B (2014) A new chitinase-producer strain Streptomyces glauciniger WICC-A03: isolation and identification as a biocontrol agent for plants phytopathogenic fungi. Nat Prod Res 28(24):2273–2277CrossRefGoogle Scholar
  12. Bailey K, Lazarovits G (2003) Suppressing soil-borne diseases with residue management and organic amendments. Soil Tillage Res 72(2):169–180CrossRefGoogle Scholar
  13. Banerjee MR, Yesmin L, Vessey JK (2006) Plant-growth-promoting rhizobacteria as biofertilizers and biopesticides, Handbook of microbial biofertilizers. Food Products Press, New York, pp 137–181Google Scholar
  14. Bauermeister A, Amador IR, Pretti CP, Giese EC, Oliveira AL, Alves da Cunha MA et al (2015) β-(1→3)-Glucanolytic yeasts from Brazilian grape microbiota: production and characterization of β-Glucanolytic enzymes by Aureobasidium pullulans 1WA1 cultivated on fungal mycelium. J Agric Food Chem 63(1):269–278CrossRefGoogle Scholar
  15. Baysal O, Lai D, Xu HH, Siragusa M, Caliskan M, Carimi F et al (2013) A proteomic approach provides new insights into the control of soil-borne plant pathogens by Bacillus species. PLoS One 8(1):e53182. CrossRefGoogle Scholar
  16. Bent AF (1999) Applications of molecular biology to plant disease and insect resistance. Adv Agron 66:251–298CrossRefGoogle Scholar
  17. Ben-Yephet Y, Nelson EB (1999) Differential suppression of damping-off caused by Pythium aphanidermatum, P. irregulare, and P. myriotylum in composts at different temperatures. Plant Dis 83(4):356–360CrossRefGoogle Scholar
  18. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29(4):795–811CrossRefGoogle Scholar
  19. Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem 43(1):1–8CrossRefGoogle Scholar
  20. Castoria R, De Curtis F, Lima G, Caputo L, Pacifico S, De Cicco V (2001) Aureobasidium pullulans (LS-30) an antagonist of postharvest pathogens of fruits: study on its modes of action. Postharvest Biol Technol 22(1):7–17CrossRefGoogle Scholar
  21. Chaube H, Pundhir V (2005) Crop diseases and their management. PHI Learning Pvt. Ltd, New DelhiGoogle Scholar
  22. Cheuk W, Lo KV, Branion R, Fraser B, Copeman R, Jolliffe P (2003) Applying compost to suppress tomato disease. Biocycle 44(1):50–51Google Scholar
  23. Coventry E, Noble R, Whipps J (2001) Composting of onion and other vegetable wastes, with particular reference to Allium white rot. Rep Community Supported Agric 4862:1–95Google Scholar
  24. Coventry E, Noble R, Mead A, Whipps J (2002) Control of Allium white rot (Sclerotium cepivorum) with composted onion waste. Soil Biol Biochem 34(7):1037–1045CrossRefGoogle Scholar
  25. Daguerre Y, Siegel K, Edel-Hermann V, Steinberg C (2014) Fungal proteins and genes associated with biocontrol mechanisms of soil-borne pathogens: a review. Fungal Biol Rev 28(4):97–125CrossRefGoogle Scholar
  26. Dissanayake N, Hoy J (1999) Organic material soil amendment effects on root rot and sugarcane growth and characterization of the materials. Plant Dis 83(11):1039–1046CrossRefGoogle Scholar
  27. El-Mehalawy AA, Hassanein NM, Khater HM, El-Din EK, Youssef YA (2004) Influence of maize root colonization by the rhizosphere actinomycetes and yeast fungi on plant growth and on the biological control of late wilt disease. Int J Agric Biol 6(4):599–605Google Scholar
  28. El-Tarabily K (2004) Suppression of Rhizoctonia solani diseases of sugar beet by antagonistic and plant growth-promoting yeasts. J Appl Microbiol 96(1):69–75CrossRefGoogle Scholar
  29. Emmert EA, Handelsman J (1999) Biocontrol of plant disease: a gram positive perspective. FEMS Microbiol Lett 171(1):1–9CrossRefGoogle Scholar
  30. Falih A, Wainwright M (1995) Nitrification, S-oxidation and P-solubilization by the soil yeast Williopsis californica and by Saccharomyces cerevisiae. Mycol Res 99(2):200–204CrossRefGoogle Scholar
  31. Ferrara A;Avataneo M, Nappi P (1996) First experiments of compost suppressiveness to some phytopathogens. In The science of composting. Springer, Heidelberg, pp 1157–1160Google Scholar
  32. Ferrreira RMSB, Freitas RFL, Monteiro SAVS (2012) Targeting carbohydrates: a novel paradigm for fungal control. Eur J Plant Pathol 133(1):117–140CrossRefGoogle Scholar
  33. Fu SF, Sun PF, Lu HY, Wei JY, Xiao HS, Fang WT et al (2016) Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of Drosera spatulata Lab. Fungal Biol 120(3):433–448CrossRefGoogle Scholar
  34. Fuchs J (2002) Practical use of quality compost for plant health and vitality improvement. In Microbiology of composting. Springer, Heidelberg, pp 435–444Google Scholar
  35. Gomiero T, Paoletti M, Pimentel D (2008) Energy and environmental issues in organic and conventional agriculture. Crit Rev Plant Sci 27(4):239–254CrossRefGoogle Scholar
  36. Greenfield H, Southgate DA (2003) Food composition data: production, management, and use. Food & Agriculture Organization of the United Nations, RomaGoogle Scholar
  37. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3(4):307–319CrossRefGoogle Scholar
  38. Hardy GSJ, Sivasithamparam K (1991) Suppression of Phytophthora root rot by a composted Eucalyptus bark mix. Aust J Bot 39(2):153–159CrossRefGoogle Scholar
  39. Hökeberg M (2005) Development and registration of biocontrol products-experiences and perspectives gained from the bacterial seed treatment products Cedomon® and Cerall®, DIAS report, 77. Research Centre Flakkebjerg, DenmarkGoogle Scholar
  40. Hornby D (1990) Biological control of soil-borne plant pathogens: the centre for agriculture and bioscience international. CAB International, LondonGoogle Scholar
  41. Huelsman M, Edwards C (1998) Management of disease in cucumbers (Cucumis sativus) and peppers (Capsicum annum) by using composts as fertility inputs. Food & Agriculture Organization of the United Nations, LondonGoogle Scholar
  42. Igo N (1983) Survey of greenhouse management practices in Essex County, Ontario, in relation to Fusarium foot and root rot of tomato. Plant Dis 67(1):38–40CrossRefGoogle Scholar
  43. Janisiewicz W, Tworkoski T, Sharer C (2000) Characterizing the mechanism of biological control of postharvest diseases on fruits with a simple method to study competition for nutrients. Phytopathology 90(11):1196–1200CrossRefGoogle Scholar
  44. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48(1):1–13CrossRefGoogle Scholar
  45. Kim KD, Nemec S, Musson G (1997) Effects of composts and soil amendments on soil microflora and Phytophthora root and crown rot of bell pepper. Crop Prot 16(2):165–172CrossRefGoogle Scholar
  46. Kim P, Bai H, Bai D, Chae H, Chung S, Kim Y et al (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97(5):942–949CrossRefGoogle Scholar
  47. Kreger-van RNJW (2013) The yeasts: a taxonomic study. Elsevier, Tokyo, pp 45–65Google Scholar
  48. LaMondia J, Gent M, Ferrandino F, Elmer W, Stoner K (1999) Effect of compost amendment or straw mulch on potato early dying disease. Plant Dis 83(4):361–366CrossRefGoogle Scholar
  49. Lewis J, Lumsden R, Millner P, Keinath A (1992) Suppression of damping-off of peas and cotton in the field with composted sewage sludge. Crop Prot 11(3):260–266CrossRefGoogle Scholar
  50. Liu GL, Chi Z, Wang GY, Wang ZP, Li Y, Chi ZM (2015) Yeast killer toxins, molecular mechanisms of their action and their applications. Crit Rev Biotechnol 35(2):222–234CrossRefGoogle Scholar
  51. Lucas J (2009) Plant pathology and plant pathogens. Wiley, Oxford, pp 233–249Google Scholar
  52. Lugtenberg B, Leveau J (2007) 10 biocontrol of plant pathogens: principles, promises, and pitfalls. The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, pp 267–268Google Scholar
  53. Lumsden R, Lewis J, Millner P (1983) Effect of composted sewage sludge on several soilborne pathogens and diseases. Phytopathology 73(11):1543–1548CrossRefGoogle Scholar
  54. Martin CCS, Ramsubhag A (2015) 18 potential of compost for suppressing plant diseases. Sustainable crop disease management using natural products. CAB International, Boston, pp 345–346CrossRefGoogle Scholar
  55. Masih E, Slezack-Deschaumes S, Marmaras I, Barka EA, Vernet G, Charpentier C et al (2001) Characterisation of the yeast Pichia membranifaciens and its possible use in the biological control of Botrytis cinerea, causing the grey mould disease of grapevine. FEMS Microbiol Lett 202(2):227–232CrossRefGoogle Scholar
  56. Mašínová T, Bahnmann BD, Větrovský T, Tomšovský M, Merunková K, Baldrian P (2017) Drivers of yeast community composition in the litter and soil of a temperate forest. FEMS Microbiol Ecol 93(2):fiw223. CrossRefGoogle Scholar
  57. Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and β-1, 3-glucanase. Plant Physiol 88(3):936–942CrossRefGoogle Scholar
  58. Mehta C, Gupta V, Singh S, Srivastava R, Sen E, Romantschuk M et al (2012) Role of microbiologically rich compost in reducing biotic and abiotic stresses. In: Microorganisms in environmental management. Springer, Heidelberg, pp 113–134Google Scholar
  59. Montesinos E (2003) Development, registration and commercialization of microbial pesticides for plant protection. Int Microbiol 6(4):245–252CrossRefGoogle Scholar
  60. Muccilli S, Wemhoff S, Restuccia C, Meinhardt F (2013) Exoglucanase-encoding genes from three Wickerhamomyces anomalus killer strains isolated from olive brine. Yeast 30(1):33–43CrossRefGoogle Scholar
  61. Munimbazi C, Bullerman L (1998) Isolation and partial characterization of antifungal metabolites of Bacillus pumilus. J Appl Microbiol 84(6):959–968CrossRefGoogle Scholar
  62. Nassar AH, El-Tarabily KA, Sivasithamparam K (2005) Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fertil Soils 42(2):97–108CrossRefGoogle Scholar
  63. Noble R, Coventry E (2010) Suppression of soil-borne plant diseases with composts: a review. Biocontrol Sci Tech 15(1):3–20CrossRefGoogle Scholar
  64. Oro L, Ciani M, Bizzaro D, Comitini F (2016) Evaluation of damage induced by Kwkt and Pikt zymocins against Brettanomyces/Dekkera spoilage yeast, as compared to sulphur dioxide. J Appl Microbiol 121:207–214CrossRefGoogle Scholar
  65. Pacwa PM, Płaza GA, Piotrowska SZ, Cameotra SS (2011) Environmental applications of biosurfactants. Int J Mol Sci 12(1):633–654CrossRefGoogle Scholar
  66. Pal KK, Gardener BM (2006) Biological control of plant pathogens. The Plant Health Instructor 2:1117–1142Google Scholar
  67. Paterson E, Hall J, Rattray E, Griffiths B, Ritz K, Killham K (1997) Effect of elevated CO2 on rhizosphere carbon flow and soil microbial processes. Glob Chang Biol 3(4):363–377CrossRefGoogle Scholar
  68. Pera A, Filippi C (1987) Controlling of Fusarium wilt in carnation with bark compost. Biological Wastes 22(3):219–228CrossRefGoogle Scholar
  69. Perez MF, Contreras L, Garnica NM, Fernández-Zenoff MV, Farías ME, Sepulveda M et al (2016) Native killer yeasts as biocontrol agents of postharvest fungal diseases in lemons. PLoS One 11(10):e0165590. CrossRefGoogle Scholar
  70. Quimby P, King L, Grey W (2002) Biological control as a means of enhancing the sustainability of crop/land management systems. Agric Ecosyst Environ 88(2):147–152CrossRefGoogle Scholar
  71. Sansone G, Rezza I, Calvente V, Benuzzi D, de Tosetti MIS (2005) Control of Botrytis cinerea strains resistant to iprodione in apple with rhodotorulic acid and yeasts. Postharvest Biol Technol 35(3):245–251CrossRefGoogle Scholar
  72. Schuler C, Pikny J, Nasir M, Vogtmann H (1993) Effects of composted organic kitchen and garden waste on Mycosphaerella pinodes (Berk. et Blox) Vestergr., causal organism of foot rot on peas (Pisum sativum L.). Biological Agriculture and Horticulture, LondonGoogle Scholar
  73. Serra WC, Houot S, Alabouvette C (1996) Increased soil suppressiveness to Fusarium wilt of flax after addition of municipal solid waste compost. Soil Biol Biochem 28(9):1207–1214CrossRefGoogle Scholar
  74. Simsek EY (2011) The use of vermicompost products to control plant diseases and pests. In: Biology of earthworms. Springer, Berlin, pp 191–213Google Scholar
  75. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56(4):845–857CrossRefGoogle Scholar
  76. Stone A, Vallad G, Cooperband L, Rotenberg D, Darby H, James R et al (2003) Effect of organic amendments on soilborne and foliar diseases in field-grown snap bean and cucumber. Plant Dis 87(9):1037–1042CrossRefGoogle Scholar
  77. Suzzi G, Romano P, Ponti I, Montuschi C (1995) Natural wine yeasts as biocontrol agents. J Appl Bacteriol 78(3):304–308CrossRefGoogle Scholar
  78. Thangavelu R, Mustaffa M (2012) Current advances in the Fusarium wilt disease management in banana with emphasis on biological control. INTECH, Shanghai, pp 274–287Google Scholar
  79. Tilston E, Pitt D, Groenhof A (2002) Composted recycled organic matter suppresses soil-borne diseases of field crops. New Phytol 154(3):731–740CrossRefGoogle Scholar
  80. Urquhart E, Punja Z (2002) Hydrolytic enzymes and antifungal compounds produced by Tilletiopsis species, phyllosphere yeasts that are antagonists of powdery mildew fungi. Can J Microbiol 48(3):219–229CrossRefGoogle Scholar
  81. Van Os G, Van Ginkel J (2001) Suppression of pythium root rot in bulbous iris in relation to biomass and activity of the soil microflora. Soil Biol Biochem 33(11):1447–1454CrossRefGoogle Scholar
  82. Wang S, Liang Y, Shen T, Yang H, Shen B (2016) Biological characteristics of Streptomyces albospinus CT205 and its biocontrol potential against cucumber Fusarium wilt. Biocontrol Sci Tech 26(7):951–963CrossRefGoogle Scholar
  83. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52(1):487–511CrossRefGoogle Scholar
  84. Whipps J, Gerhardson B (2007) Biological pesticides for control of seed-and soil-borne plant pathogens. Modern soil microbiology. CRC Press, Boca Raton, pp 479–501Google Scholar
  85. Widmer T, Graham J, Mitchell D (1998) Composted municipal waste reduces infection of citrus seedlings by Phytophthora nicotianae. Plant Dis 82(6):683–688CrossRefGoogle Scholar
  86. Widmer T, Graham J, Mitchell D (1999) Composted municipal solid wastes promote growth of young citrus trees infested with Phytophthora nicotianae. Compost Science & Utilization 7(2):6–16CrossRefGoogle Scholar
  87. Willer H, Yussefi M, Sorensen N (2010) The world of organic agriculture. Statistics and emerging trends 2008. IFOAM, Earthscan, LondonGoogle Scholar
  88. Wisniewski M, Biles C, Droby S, McLaughlin R, Wilson C, Chalutz E (1991) Mode of action of the postharvest biocontrol yeast, Pichia guilliermondii. I. Characterization of attachment to Botrytis cinerea. Physiol Mol Plant Pathol 39(4):245–258CrossRefGoogle Scholar
  89. Young IM, Blanchart E, Chenu C, Dangerfield M, Fragoso C, Grimaldi M et al (1998) The interaction of soil biota and soil structure under global change. Glob Chang Biol 4(7):703–712CrossRefGoogle Scholar
  90. Youssef SA, Tartoura KA (2013) Compost enhances plant resistance against the bacterial wilt pathogen Ralstonia solanacearum via up-regulation of ascorbate-glutathione redox cycle. Eur J Plant Pathol 137(4):821–834CrossRefGoogle Scholar
  91. Yuliar, Nion YA, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ 30(1):1–11CrossRefGoogle Scholar
  92. Zaidi NW, Singh US (2013) 14 Trichodermain plant health management. Trichoderma: biology and applications. CAB International, London, p 230CrossRefGoogle Scholar
  93. Zhang L (2000) Biological fertilizer based on yeasts. US Patent, US6416983, September 5, 2000Google Scholar
  94. Zhao J, Teixeira da Silva J (2006) Elicitor signal transduction leading to biosynthesis of plant defensive secondary metabolites. Floriculture, ornamental and plant biotechnology. Global Science Books, Ltd, Tokyo, pp 344–357Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Azzam Aladdin
    • 1
  • Julián Rafael Dib
    • 2
    • 3
  • Roslinda Abd. Malek
    • 1
  • Hesham A. El Enshasy
    • 1
    Email author
  1. 1.Institute of Bioproduct Development (IBD)Universiti Teknologi MalaysiaJohor BahruMalaysia
  2. 2.Planta Piloto de Procesos Industriales Microbiológicos (PROIMI-CONICET)TucumánArgentina
  3. 3.Instituto de Microbiología, Facultad de Bioquimica, Quimica y FarmaciaUniversidad Nacional de TucumánTucumánArgentina

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