Applied Microbiology and Biotechnology

, Volume 97, Issue 17, pp 7579–7585

The safety assessment of Pythium irregulare as a producer of biomass and eicosapentaenoic acid for use in dietary supplements and food ingredients

Mini-Review

Abstract

Polyunsaturated fatty acids, docosahexaenoic acid (DHA, 22:6, n-3), eicosapentaenoic acid (EPA, 20:5, n-3), and arachidonic acid (ARA, 20:4 n-6), have multiple beneficial effects on human health and can be used as an important ingredient in dietary supplements, food, feed and pharmaceuticals. A variety of microorganisms has been used for commercial production of these fatty acids. The microorganisms in the Pythium family, particularly Pythium irregulare, are potential EPA producers. The aim of this work is to provide a safety assessment of P. irregulare so that the EPA derived from this species can be potentially used in various commercial applications. The genus Pythium has been widely recognized as a plant pathogen by infecting roots and colonizing the vascular tissues of various plants such as soybeans, corn and various vegetables. However, the majority of the Pythium species (including P. irregulare) have not been reported to infect mammals including humans. The only species among the Pythium family that infects mammals is P. insidiosum. There also have been no reports showing P. irregulare to contain mycotoxins or cause potentially allergenic responses in humans. Based on the safety assessment, we conclude that P. irregulare can be considered a safe source of biomass and EPA-containing oil for use as ingredients in dietary supplements, food, feed and pharmaceuticals.

Keywords

Safety assessment Pythium irregulare Oomycete Eicosapentaenoic acid (EPA) Algae 

References

  1. Abad ZG, Louws FJ, Fernandez GE (1999) Rhizoctonia and Pythium species associated with black root rot of strawberries in North Carolina. Phytopathology 89:S1CrossRefGoogle Scholar
  2. Abbasi PA, Lazarovits G (2006) Effect of soil application of AG3 phosphonate on the severity of clubroot of bok choy and cabbage caused by Plasmodiophora brassicae. Plant Dis 90:1517–1522CrossRefGoogle Scholar
  3. Aldahadha AM, Warwick NWM, Backhouse D (2012) Effects of Pythium irregulare and root pruning on water-use efficiency of hydroponically grown wheat under PEG-induced drought. J Phytopathol 160:397–403CrossRefGoogle Scholar
  4. Athalye SK, Garcia RA, Wen ZY (2009) Use of biodiesel-derived crude glycerol for producing eicosapentaenoic acid (EPA) by the fungus Pythium irregulare. J Agri Food Chem 57:2739–2744CrossRefGoogle Scholar
  5. Bala K, Robideau GP, Desaulniers N, de Cock AWAM, Levesque CA (2010) Taxonomy, DNA barcoding and phylogeny of three new species of Pythium from Canada. Persoonia 25:22–31PubMedCrossRefGoogle Scholar
  6. Belarbi EH, Molina E, Chisti Y (2000) A process for high yield and scaleable recovery of high purity eicosapentaenoic acid esters from microalgae and fish oil. Enzyme Microb Technol 26:516–529PubMedCrossRefGoogle Scholar
  7. Biesbroc J, Hendrix FF (1967) A taxonomic study of Pythium irregulare and related species. Mycologia 59:943–952CrossRefGoogle Scholar
  8. Blunt TD, Ambruzs B, Brown W (2001) Re-emergence of red root rot of corn in Colorado. Phytopathology 91:S9Google Scholar
  9. Bracco U, Deckelbaum RJ (1992) Polyunsaturated fatty acid in human nutrition. Raven Press, LondonGoogle Scholar
  10. Brenna JT, Salem NJ, Sinclair AJ, Cunnane SC (2009) Alpha-linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fat Acids 80:85–91CrossRefGoogle Scholar
  11. Broders KD, Lipps PE, Ellis ML, Dorrance AE (2009) Pythium delawarii—a new species isolated from soybean in Ohio. Mycologia 101:232–238PubMedCrossRefGoogle Scholar
  12. Burgess LW, Knight TE, Tesoriero L, Phan HT (2008) Fungi, humans and animals: health issues. In: Diagnostic manual for plant diseases in Vietnam. ACIAR (Australian Centre for International Agricultural Research), Canberra, Australia. Pp 162–170Google Scholar
  13. Chen WD (1992) Restriction-fragment-length-polymorphisms in enzymatically amplified ribosomal DNAs of 3 Heterothallic Pythium species. Phytopathology 82:1467–1472CrossRefGoogle Scholar
  14. Cheng MH, Walker TH, Hulbert GJ, Raman DR (1999) Fungal production of eicosapentaenoic and arachidonic acids from industrial waste streams and crude soybean oil. Biores Technol 67:101–110CrossRefGoogle Scholar
  15. Cohen Z, Ratledge C (2010) Single cell oils, 2nd edn. AOCS Press, UrbanaGoogle Scholar
  16. Dodds PN, Rafiqi M, Gan PHP, Hardham AR, Jones DA, Ellis JG (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytol 183:993–999PubMedCrossRefGoogle Scholar
  17. Dong M, Walker TH (2008) Addition of polyunsaturated fatty acids to canola oil by fungal conversion. Enzyme Micro Technol 42:514–520CrossRefGoogle Scholar
  18. Dorrance AE, Berry SA, Bowen P, Lipps PE (2004) Characterization of Pythium spp. from three Ohio fields for pathogenicity on corn and soybean and metalaxyl sensitivity. Plant Health Progress 2:1–7Google Scholar
  19. Eroshin VK, Satroutdinov AD, Dedyukhina EG, Chistyakova TI (2000) Arachidonic acid production by Mortierella alpina with growth-coupled lipid synthesis. Proc Biochem 35:1171–1175CrossRefGoogle Scholar
  20. FDA (2011) GRAS Notice Inventory (GRN No. 355), Eicosapentaenoic acid (EPA)-rich triglyceride oil from Yarrowia lipolytica. http://www.accessdata.fda.gov/scripts/fcn/fcnDetailNavigation.cfm?rpt=graslisting&id=355Forbes. Accessed 28 May 2013
  21. Forbes GA, Davet P (1990) Characterization and pathogenicity on seedlings of Pythium species Isolated from soybean roots in the toulouse area. Agronomie 10:825–830CrossRefGoogle Scholar
  22. Gaastra W, Lipman LJA, de Cock AWAM, Exel TK, Pegge RBG, Scheurwater J, Vilela R, Mendoza L (2010) Pythium insidiosum: an overview. Vet Microbiol 146:1–16PubMedCrossRefGoogle Scholar
  23. Gandhi SR, Weete JD (1991) Production of the polyunsaturated fatty-acids arachidonic-acid and eicosapentaenoic acid by the fungus Pythium-ultimum. J Gen Microbiol 137:1825–1830PubMedCrossRefGoogle Scholar
  24. Garzon CD, Yanez JM, Moorman GW (2007) Pythium cryptoirregulare, a new species within the P-irregulare complex. Mycologia 99:291–301PubMedCrossRefGoogle Scholar
  25. GBIF (2008). Biodiversity Information Facility. http://data.gbif.org/species/Global; Accessed 28 May 2013
  26. Gibson RA, Muhlhausler B, Makrides M (2011) Conversion of linoleic acid and alpha-linolenic aicd to long-chain polyunsaturated fatty acid (LCPUFAs), with a focus on pregnency, lactation and the first 2 years of life. Matern Child Nutr 7(suppl 2):17–26PubMedCrossRefGoogle Scholar
  27. Gill I, Valivety R (1997) Polyunsaturated fatty acids: Part 1. Occurrence, biological activities and applications. Trends Biotechnol 15:401–409PubMedCrossRefGoogle Scholar
  28. Gupta A, Barrow CJ, Puri M (2012) Omega-3 biotechnology: thraustochytrids as a novel source of omega-3 oils. Biotechnol Adv 30:1733–1745PubMedCrossRefGoogle Scholar
  29. Grammatikos SI, Subbaiah PV, Victor TA, Miller WM (1994) Diverse effects of essential (N-6 and N-3) fatty-acids on cultured-cells. Cytotechnology 15:31–50PubMedCrossRefGoogle Scholar
  30. Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann Bot 80:713–720CrossRefGoogle Scholar
  31. Herrero ML, Hermansen A, Elen ON (2003) Occurrence of Pythium spp. and phytophthora spp. in Norwegian greenhouses and their pathogenicity on cucumber seedlings. J Phytopathol Phytopath Z 151:36–41CrossRefGoogle Scholar
  32. Ivanov DA, Bernards MA (2012) Ginsenosidases and the pathogenicity of Pythium irregulare. Phytochemistry 78:44–53PubMedCrossRefGoogle Scholar
  33. Jiang YN, Haudenshield JS, Hartman GL (2012) Characterization of Pythium spp. from soil samples in Illinois. Can J Plant Pathol Rev Can Phytopathol 34:448–454CrossRefGoogle Scholar
  34. Kabak B, Dobson ADW (2009) Biological strategies to counteract the effects of mycotoxins. J Food Protect 72:2006–2016Google Scholar
  35. Koike Y, Cai HJ, Higashiyama K, Fujikawa S, Park EY (2001) Effect of consumed carbon to nitrogen ratio of mycelial morphology and arachidonic acid production in cultures of Mortierella alpine. J Biosci Bioeng 91:382–389PubMedGoogle Scholar
  36. Lan W, Qin W, Yu L (2002) Effect of glutamate on arachidonic acid production from Mortierella alpine. Lett Appl Microbiol 35:357–360PubMedCrossRefGoogle Scholar
  37. Levesque CA, de Cock AWAM (2004) Molecular phylogeny and taxonomy of the genus Pythium. Mycol Res 108:1363–1383PubMedCrossRefGoogle Scholar
  38. Li DW, Yang CS (2004) Fungal contamination as a major contributor to sick building syndrome. Adv Appl Microbiol 55:31–112PubMedCrossRefGoogle Scholar
  39. Liang Y, Garcia RA, Piazza GJ, Wen ZY (2011) Nonfeed application of rendered animal proteins for microbial production of eicosapentaenoic acid by the fungus Pythium irregulare. J Agri Food Chem 59:11990–11996CrossRefGoogle Scholar
  40. Liang Y, Zhao XF, Strait M, Wen ZY (2012) Use of dry-milling derived thin stillage for producing eicosapentaenoic acid (EPA) by the fungus Pythium irregulare. Biores Technol 111:404–409CrossRefGoogle Scholar
  41. Lio JY, Wang T (2013) Pythium irregulare fermentation to produce arachidonic acid (ARA) and eicosapentaenoic acid (EPA) using soybean processing co-products as substrates. Appl Biochem Biotechnol 169:595–611PubMedCrossRefGoogle Scholar
  42. Mao W, Carroll RB, Whittington DP (1993) Assessment of soil populations of Phoma, Pythium irregulare and Fusarium sp. associated with red root rot of corn in Delaware. Phytopathology 83:1407Google Scholar
  43. Masih I, Paul B (2003) Pythium irregulare sp. nov., isolated from the Canary Islands, its taxonomy, its region of rDNA, and comparison with related species. Curr Microbiol 47:309–313PubMedCrossRefGoogle Scholar
  44. Matsumoto C, Kageyama K, Suga H, Hyakumachi M (2000) Intraspecific DNA polymorphisms of Pythium irregulare. Mycol Res 104:1333–1341CrossRefGoogle Scholar
  45. Mazzola M, Andrews PK, Reganold JP, Levesque CA (2002) Frequency, virulence, and metalaxyl sensitivity of Pythium spp. isolated from apple roots under conventional and organic production systems. Plant Dis 86:669–675CrossRefGoogle Scholar
  46. Mazzola M, Brown J, Zhao XW, Izzo AD, Fazio G (2009) Interaction of brassicaceous seed meal and apple rootstock on recovery of Pythium spp. and Pratylenchus penetrans from roots grown in replant soils. Plant Dis 93:51–57CrossRefGoogle Scholar
  47. Mazzola M, Manici LM (2012) Apple replant disease: role of microbial ecology in cause and control. Annu Rev Phytopathol 50:45–65PubMedCrossRefGoogle Scholar
  48. Mendes A, Reis A, Vasconcelos R, Guerra P, da Silva TL (2009) Crypthecodinium cohnii with emphasis on DHA production: a review. J Appl Phycol 21:199–214CrossRefGoogle Scholar
  49. McLeod A, Botha WJ, Meitz JC, Spies CFJ, Tewoldemedhin YT, Mostert L (2009) Morphological and phylogenetic analyses of Pythium species in South Africa. Mycol Res 113:933–951PubMedCrossRefGoogle Scholar
  50. Mojdehi H, Singleton LL, Melouk HA, Waller GR (1990) Reproduction of symptoms of a root disease of wheat by toxic metabolites produced by 2 Pythium species and their partial characterization. J Phytopathol Phytopath Z 128:246–256CrossRefGoogle Scholar
  51. Mojdehi H, Singleton LL (2000) Reaction of wheat varieties to infection by Pythium arrhenomanes or its toxic metabolite(s). J Agric Sci Technol 1:33–39Google Scholar
  52. Moorman GW, Kang S, Geiser DM, Kim SH (2002) Identification and characterization of Pythium species associated with greenhouse floral crops in Pennsylvania. Plant Dis 86:1227–1231CrossRefGoogle Scholar
  53. Nettleton JA (1995) Omega-3 fatty acids and health. Chapman & Hall, New YorkCrossRefGoogle Scholar
  54. Olaya G, Heidel T, Abad G, Abad J, Watrin C (2006) Pythium species associated with corn seedling diseases in the USA, pathogenicity and sensitivity to mefenoxam and azoxystrobin. Phytopathology 96:S87CrossRefGoogle Scholar
  55. Paul B (2000) ITS1 region of the rDNA of Pythium megacarpum sp. nov., its taxonomy, and its comparison with related species. FEMS Microbiol Lett 186:229–233PubMedCrossRefGoogle Scholar
  56. Paul B (2003) Characterisation of a new species of Pythium isolated from a wheat field in northern France and its antagonism towards Botrytis cinerea causing the grey mould disease of the grapevine. FEMS Microbiol Lett 224:215–223PubMedCrossRefGoogle Scholar
  57. Paulitz TC, Adams K (2003) Composition and distribution of Pythium communities in wheat fields in eastern Washington state. Phytopathology 93:867–873PubMedCrossRefGoogle Scholar
  58. Punja ZK, Utkhede RS (2003) Using fungi and yeasts to manage vegetable crop diseases. Trends Biotechnol 21:400–407PubMedCrossRefGoogle Scholar
  59. Rizvi SSA, Yang XB (1996) Fungi associated with soybean seedling disease in Iowa. Plant Dis 80:57–60CrossRefGoogle Scholar
  60. Robertson GI (1976) Pythium species in market gardens and their pathogenicity to 14 vegetable crops. New Zeal J Agri Res 19:97–102CrossRefGoogle Scholar
  61. Ryan AS, Zeller S, Nelson EB (2010) Safety evaluation o fsingle cell oils and the regulatory requirements for use as food ingredients. In: Cohen Z, Ratledge C (eds) Single cell oils, 2nd edn. AOCS Press, Urbana, pp 317–350Google Scholar
  62. Schurko AM, Mendoza L, Levesque CA, Desaulniers NL, de Cock WAM, Klassen GR (2003) A molecular phylogeny of Pythium insidiosum. Mycol Res 107:537–544PubMedCrossRefGoogle Scholar
  63. Serrano Y, Gomez JM, Melero-Vara JM, Abad Z (2009) Pythium species causing green bean diseases in plastic greenhouses in southeast Spain. Phytopathology 99:S118Google Scholar
  64. Shimizu S, Kawashima H, Shinmen Y, Akimoto K, Yamada H (1988) Production of eicosapentaenoic acid by mortierella fungi. J Ameri Oil Chem Soc 65:1455–1459CrossRefGoogle Scholar
  65. Simopoulos AP (1999) Essential fatty acids in health and chronic disease. Am J Clin Nutr 70:560S–569SPubMedGoogle Scholar
  66. Smither ML, Jones AL (1989) Pythium species associated with sour cherry and the effect of P. irregulare on the growth of mahaleb cherry. Can J Plant Pathol Rev Can Phytopathol 11:1–8CrossRefGoogle Scholar
  67. Stredansky M, Conti E, Salaris A (2000) Production of polyunsaturated fatty acids by Pythium ultimum in solid-state cultivation. Enzyme Micro Technol 26:304–307CrossRefGoogle Scholar
  68. Tewoldemedhin YT, Mazzola M, Botha WJ, Spies CFJ, McLeod A (2011) Characterization of fungi (Fusarium and Rhizoctonia) and oomycetes (Phytophthora and Pythium) associated with apple orchards in South Africa. Eur J Plant Pathol 130:215–229CrossRefGoogle Scholar
  69. Vanderplaatsniterink AJ (1981) Monograph of the genus Pythium. Stud Mycol 21:1–242Google Scholar
  70. Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159:93–100CrossRefGoogle Scholar
  71. Ward OP, Singh A (2005) Omega-3/6 fatty acids: alternative sources of production. Process Biochem 40:3627–3652CrossRefGoogle Scholar
  72. Wen ZY, Chen F (2003) Heterotrophic production of eicosapentaenoic acid by microalgae. Biotechnol Adv 21:273–294PubMedCrossRefGoogle Scholar
  73. Zhu M, Yu L-J, Wu Y-X (2003) An inexpensive medium for production of arachidonic acid by Mortierella alpine. J Ind Microbiol Biotechnol 30:75–79PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Food Science and Human NutritionIowa State UniversityAmesUSA
  2. 2.AlgiSys, LLCClevelandUSA

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