Direct fungal fermentation of lignocellulosic biomass into itaconic, fumaric, and malic acids: current and future prospects

Mini-Review

Abstract

Various economic and environmental sustainability concerns as well as consumer preference for bio-based products from natural sources have paved the way for the development and expansion of biorefining technologies. These involve the conversion of renewable biomass feedstock to fuels and chemicals using biological systems as alternatives to petroleum-based products. Filamentous fungi possess an expansive portfolio of products including the multifunctional organic acids itaconic, fumaric, and malic acids that have wide-ranging current applications and potentially addressable markets as platform chemicals. However, current bioprocessing technologies for the production of these compounds are mostly based on submerged fermentation, which necessitates physicochemical pretreatment and hydrolysis of lignocellulose biomass to soluble fermentable sugars in liquid media. This review will focus on current research work on fungal production of itaconic, fumaric, and malic acids and perspectives on the potential application of solid-state fungal cultivation techniques for the consolidated hydrolysis and organic acid fermentation of lignocellulosic biomass.

Keywords

Fungi Solid-state fermentation Biomass Bio-based chemicals Simultaneous hydrolysis and fermentation Mixed cultures Valorization 

References

  1. 1.
    Abe S, Furuya A, Saito T, Takayama K (1962) Method of producing L-malic acid by fermentation. United States Patent 3,063,910Google Scholar
  2. 2.
    Alonso L, Parajo JC, Moldes AB (2001) Strategies to improve the bioconversion of processed wood into lactic acid by simultaneous saccharification and fermentation. J Chem Technol Biotechnol 76:279–284Google Scholar
  3. 3.
    Anuradha R, Suresh AK, Venkatesh KV (1999) Simultaneous saccharification and fermentation of starch to lactic acid. Process Biochem 35:367–375Google Scholar
  4. 4.
    Baldrian P, Val V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521PubMedGoogle Scholar
  5. 5.
    Battat E, Peleg Y, Bercovitz A et al (1991) Optimization of L-malic acid production by Aspergillus flavus in a stirred fermenter. Biotechnol Bioeng 27:1108–1116Google Scholar
  6. 6.
    Bellon-Maurel V, Orliac O, Christen P (2003) Sensors and measurements in solid state fermentation: a review. Process Biochem 38:881–896Google Scholar
  7. 7.
    Bentley R, Thiessen CP (1957) Biosynthesis of itaconic acid in Aspergillus terreus: II. Early stages in glucose dissimilation and the role of citrate. J Biol Chem 226:689–701PubMedGoogle Scholar
  8. 8.
    Braun S, Vecht-Lifshitz S (1991) Mycelial morphology and metabolite production. Trends Biotechnol 9:63–68Google Scholar
  9. 9.
    Bressler E, Braun S (2000) Conversion of citric acid to itaconic acid in a novel liquid membrane bioreactor. J Chem Technol Biotechnol 75:66–72Google Scholar
  10. 10.
    Brijwani K, Oberoi HS, Vadlani PV (2010) Production of a cellulolytic enzyme system in mixed-culture solid-state fermentation of soybean hulls supplemented with wheat bran. Process Biochem 45:120–128Google Scholar
  11. 11.
    Brijwani K, Vadlani PV (2011) Solid state fermentation of soybean hulls for cellulolytic enzymes production. In: Ng T-B (ed) Soybean applications andtechnology. InTech, Shanghai, pp 305–322Google Scholar
  12. 12.
    Brock BJ, Rielbe S, Gold MH (1995) Purification and characterization of 1,4-benzoquinone reductase from the basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 61:3076–3081PubMedCentralPubMedGoogle Scholar
  13. 13.
    Byrne G, Ward O (1989) Effect of nutrition on pellet formation by Rhizopus arrhizus. Biotechnol Bioeng 33:912–914PubMedGoogle Scholar
  14. 14.
    Calam CT, Oxford AE, Raistrick H (1939) The biochemistry of microorganisms LXIII. Itaconic acid, a metabolic product of a strain of Aspergillus terreusthom. Biochem J 33:1488–1495PubMedCentralPubMedGoogle Scholar
  15. 15.
    Cao N, Du J, Gong CS, Tsao GT (1996) Simultaneous production and recovery of fumaric acid from immobilized Rhizopus oryzae with a rotary biofilm contactor and an adsorption Column. Appl Environ Microbiol 62:2926–2931PubMedCentralPubMedGoogle Scholar
  16. 16.
    Cao N, Du J, Chen C et al (1997) Production of fumaric acid by immobilized Rhizopus using rotary biofilm contactor. Appl Biochem Biotechnol 63–65:387–394PubMedGoogle Scholar
  17. 17.
    Carere CR, Sparling R, Cicek N, Levin DB (2008) Third generation biofuels via direct cellulose fermentation. Int J Mol Sci 9:1342–1360PubMedCentralPubMedGoogle Scholar
  18. 18.
    Carta FS, Soccol CR, Ramos LP, Fontana JD (1999) Production of fumaric acid by fermentation of enzymatic hydrolysates derived from cassava bagasse. Bioresour Technol 68:23–28Google Scholar
  19. 19.
    Chahal DS (1985) Solid-state fermentation with Trichoderma reesei for cellulase production. Appl Environ Microbiol 49:205–210PubMedCentralPubMedGoogle Scholar
  20. 20.
    Corte-Real M, Leao C (1990) Transport of malic acid and other dicarboxylic acids in the yeast Hansenula anomala. Appl Environ Microbiol 56:1109–1113PubMedCentralPubMedGoogle Scholar
  21. 21.
    Cunha FM, Bacchin ALG, Horta ACL et al (2012) Indirect method for quantification of cellular biomass in a solidscontaining medium used as pre-culture for cellulase production. Biotechnol Bioprocess Eng 17:100–108Google Scholar
  22. 22.
    D’Souza J, Volfova O (1982) The Effect of pH on the production of cellulases in Aspergillus terreus. Eur J Appl Microbiol Biotechnol 16:123–125Google Scholar
  23. 23.
    Dalsenter FDH, Viccini G, Barga MC et al (2005) A mathematical model describing the effect of temperature variations on the kinetics of microbial growth in solid-state culture. Process Biochem 40:801–807Google Scholar
  24. 24.
    Dashtban M, Schraft H, Qin W (2009) Fungal bioconversion of lignocellulosic residues; opportunities & perspectives. Int J Biol Sci 5:578–595PubMedCentralPubMedGoogle Scholar
  25. 25.
    Deshusses MA (1997) Biological waste air treatment in biofilters. Curr Opin Biotechnol 8:335–339PubMedGoogle Scholar
  26. 26.
    Du J, Cao N, Gong CS et al (1997) Fumaric acid production in airlift loop reactor with porous sparger. Appl Biochem Biotechnol 63–65:541–556PubMedGoogle Scholar
  27. 27.
    Du L, Jia S, Lu F (2003) Morphological changes in Rhizopus chinesis 12 in submerged culture and its relationship with antibiotic production. Process Biochem 38:1643–1646Google Scholar
  28. 28.
    Duenas R, Tengerdy RP, Gutiérrez-Correa M (1995) Cellulase production by mixed fungi in fermentation of bagasse. World J Microbiol Biotechnol 11:333–337PubMedGoogle Scholar
  29. 29.
    El-Enshasy H, Kleine J, Rinas U (2006) Agitation effects on morphology and protein productive fractions of filamentous and pelleted growth forms of recombinant Aspergillus niger. Process Biochem 41:2103–2112Google Scholar
  30. 30.
    El-Enshasy H (2007) Filamentous fungal cultures- process characteristics, products, and applications. In: Yang S (ed) Bioprocessing forvalue-added products from renewable resources—newtechnologies and applications. Elsevier, Amsterdam, pp 225–261Google Scholar
  31. 31.
    Fang H, Zhao C, Song X-Y et al (2013) Enhanced cellulolytic enzyme production by the synergism between Trichoderma reesei RUT-C30 and Aspergillus niger NL02 and by the addition of surfactants. Biotechnol Bioprocess Eng 18:390–398Google Scholar
  32. 32.
    Ferreira JA, Lennartsson PR, Edebo L, Taherzadeh MJ (2013) Zygomycetes-based biorefinery: present status and future prospects. Bioresour Technol 135:523–532PubMedGoogle Scholar
  33. 33.
    Figueiredo Z, Carvalo L Jr (1991) L-malic acid production using immobilized Saccharomyces cerevisiae. Appl Microbiol Biotechnol 30:214–217Google Scholar
  34. 34.
    Foong CW, Janaun J, Krishnaiah K, Prabhakar A (2009) Effect of superficial air velocity on solid state fermentation of palm kernel cake in a lab scale fermenter using locally isolated fungal strain. Ind Crops Prod 30:114–118Google Scholar
  35. 35.
    Foong CW, Krishnaiah K, Janaun J et al (2009) Heat and mass transfer studies of palm kernel cake (PKC) in fluidized bed fermenter. Ind Crops Prod 30:227–234Google Scholar
  36. 36.
    Foster JW, Waksman SA (1939) The production of fumaric acid by molds belonging to the genus Rhizopus. J Am Chem Soc 61:127–135Google Scholar
  37. 37.
    Gangl IC, Weigland WA, Keller FA (1990) Economic comparison of calcium fumarate and sodium fumarate production by Rhizopus arrhizus. Appl Biochem Biotechnol 24–25:663–677Google Scholar
  38. 38.
    Garg SK, Neelakantan S (1982) Studies on the properties of cellulase enzyme from Aspergillus terreus GN1. Biotechnol Bioeng 24:737–742PubMedGoogle Scholar
  39. 39.
    Gattinger LD, Duvnjak Z, Khan AW (1990) The use of canola meal as a substrate for xylanase production by Trichoderma reesei. Appl Microbiol Biotechnol 33:21–25Google Scholar
  40. 40.
    Ghose TK, Panda T, Bisaria VS (1985) Effect of culture phasing and mannanase on production of cellulase and hemicellulase by mixed culture of Trichoderma reesei D 1-6 and Aspergillus wentii Pt 2804. Biotechnol Bioeng 27:1353–1361PubMedGoogle Scholar
  41. 41.
    Goldberg I, Rokem JS, Pines O (2006) Organic acids: old metabolites, new themes. J Chem Technol Biotechnol 8:1601–1611Google Scholar
  42. 42.
    Gross R, Rhano K (2002) Biodegradable polymers for the environment. Science 297:803–807PubMedGoogle Scholar
  43. 43.
    Gutierrez-Correa M, Tengerdy RP (1997) Production of cellulase on sugar cane bagasse by fungal mixed culture solid substrate fermentation. Biotechnol Lett 19:665–667Google Scholar
  44. 44.
    Gutierrez-Correa M, Tengerdy RP (1998) Xylanase production by fungal mixed culture solid substrate fermentation on sugar cane bagasse. Biotechnol Lett 20:45–47Google Scholar
  45. 45.
    Gyamerah MH (1995) Oxygen requirement and energy relations of itaconic acid fermentation by Aspergillus terreus NRRL 1960. Appl Microbiol Biotechnol 44:20–26Google Scholar
  46. 46.
    Hamidi-Esfahani Z, Shojaosadati SA, Rinzema A (2004) Modelling of simultaneous effect of moisture and temperature on A. niger growth in solid-state fermentation. Biochem Eng J 21:265–272Google Scholar
  47. 47.
    Henriksson G, Johansson G, Pettersson G (2000) A critical review of cellobiose dehydrogenases. J Biotechnol 78:93–113PubMedGoogle Scholar
  48. 48.
    Hölker U, Höfer M, Lenz J (2004) Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Appl Microbiol Biotechnol 64:175–186PubMedGoogle Scholar
  49. 49.
    Horitsu H, Takahashi Y, Tsuda J et al (1983) Production of itaconic acid by Aspergillus terreus immobilized in polyacrylamide gels. Eur J Appl Microbiol Biotechnol 18:358–360Google Scholar
  50. 50.
    Horton P, Park K, Obayashi T, Nakai K (2006) Protein subcellular localization prediction with WoLF PSORT. In: Proceedings of the 4th Annual Asia Pacific Bioinformatics Conferece APBC06. Taipei, pp 39–48Google Scholar
  51. 51.
    Huang LP, Jin B, Lant P, Zhou J (2005) Simultaneous saccharification and fermentation of potato starch wastewater to lactic acid by Rhizopus oryzae and Rhizopus arrhizus. Biochem Eng J 23:265–276Google Scholar
  52. 52.
    Iluyemi FB, Hanafi MM (2009) Mycelial growth interactions and mannan-degrading enzyme activities from fungal mixed cultures grown on palm kernel cake. African J Biotechnol 8:2283–2288Google Scholar
  53. 53.
    Jahromi MF, Liang JB, Rosfarizan M et al (2011) Efficiency of rice straw lignocelluloses degradability by Aspergillus terreus ATCC 74135 in solid state fermentation. African J Biotechnol 10:4428–4434Google Scholar
  54. 54.
    Johnson KG (1990) Exocellular β-mannanases from hemicellulolytic fungi. World J Microbiol Biotechnol 6:209–217PubMedGoogle Scholar
  55. 55.
    Ju N, Wang SS (1986) Continuous production of itaconic acid by Aspergillus terreus immobilized in a porous disk bioreactor. Appl Microbiol Biotechnol 23:311–314Google Scholar
  56. 56.
    Juhász T, Kozma K, Szengyel Z, Réczey K (2003) Production of β-glucosidase in mixed culture of Aspergillus niger BKMF 1305 and Trichoderma reesei RUT C30. Food Technol Biotechnol 41:49–53Google Scholar
  57. 57.
    Kane J, Finlay A, Amann P (1945) Production of itaconic acid. United States Patent 2,835,283Google Scholar
  58. 58.
    Kautola H, Vahvaselka M, Linko Y-L, Linko P (1985) Itaconic acid production by immobilized Aspergillus terreus from xylose and glucose. Biotechnol Lett 7:167–172Google Scholar
  59. 59.
    Kautola H, Vassilev N, Linko YY (1989) Itaconic acid production by immobilized Aspergillus terreus on surcose medium. Biotechnol Lett 11:313–318Google Scholar
  60. 60.
    Kautola H, Linko Y (1989) Fumaric acid production from xylose by immobilized Rhizopus arrhizus cells. Appl Microbiol Biotechnol 31:448–452Google Scholar
  61. 61.
    Kautola H (1990) Itaconic acid production from xylose in repeated-batch and continuous bioreactors. Appl Microbiol Biotechnol 33:7–11Google Scholar
  62. 62.
    Kenealy W, Zaady E, Preez JC et al (1986) Biochemical aspects of fumaric acid accumulation by Rhizopus arrhizus. Appl Environ Microbiol 52:128–133PubMedCentralPubMedGoogle Scholar
  63. 63.
    Kennes C, Thalasso F (1998) Waste gas biotreatment technology. J Chem Technol Biotechnol 72:303–319Google Scholar
  64. 64.
    Khan AW, Lamb KA, Johnson KG (1989) Formation of enzymes required for the hydrolysis of plant cell wall polysaccharides by Trichoderma reesei. MIRCEN J 5:49–53Google Scholar
  65. 65.
    Khan MH, Alis S, Fakhur’l-Razi A, Alam Z (2007) Use of fungi for the bioconversion of rice straw into cellulase enzyme. J Environ Sci Heal B 42:381–386Google Scholar
  66. 66.
    Kinoshita K (1929) Production of itaconic acid and mannitol by Aspergillus itaconicus. J Chem Soc Japan 50:583–593Google Scholar
  67. 67.
    Klement T, Milker S, Jäger G et al (2012) Biomass pretreatment affects Ustilago maydis in producing itaconic acid. Microb Cell Fact. doi:10.1186/1475-2859-11-43 PubMedCentralPubMedGoogle Scholar
  68. 68.
    Kubicek C, Karaffa L (2006) Organic acids. In: Ratledge C, Kristiansen B (eds) Basic biotechnology. Cambridge University Press, UK, pp 359–380Google Scholar
  69. 69.
    Kurzatowski W, Torronen A, Filipek J et al (1996) Glucose-induced secretion of Trichoderma reesei xylanases. Appl Environ Microbiol 62:2859–2865Google Scholar
  70. 70.
    Levinson WE, Kurtzman CP, Kuo TM (2006) Production of itaconic acid by Pseudozyma antarctica NRRL Y-7808 under nitrogen-limited growth conditions. Enzyme Microb Technol 39:824–827Google Scholar
  71. 71.
    Liao W, Liu Y, Frear C, Chen S (2008) Co-production of fumaric acid and chitin from a nitrogen-rich lignocellulosic material—dairy manure—using a pelletized filamentous fungus Rhizopus oryzae ATCC 20344. Bioresour Technol 99:5859–5866PubMedGoogle Scholar
  72. 72.
    Ling L, Ng T (1989) Fermentation process for carboxylic acids. United States Patent 4,877,731Google Scholar
  73. 73.
    Lockwood LB, Ward GE (1945) Fermentation process for itaconic acid. Ind Eng Chem 37:405–406Google Scholar
  74. 74.
    Lohbeck K, Haferkorn H, Fuhrmann W, Fedtke N (1990) Maleic and fumaric acids. Ullmann’s encyclopedia of industrial chemistry, vol A16. VCH, Weinham, Germany, pp 53–62Google Scholar
  75. 75.
    Lu J, Weerasiri RR, Liu Y et al (2013) Enzyme production by the mixed fungal culture with nano-shear pretreated biomass and lignocellulose hydrolysis. Biotechnol Bioeng 110:2123–2130PubMedGoogle Scholar
  76. 76.
    Magnuson JK, Lasure LL (2004) Organic acid production by filamentous fungi. In: Lange J, Lange L (eds) Advances in fungal biotechnology for industry, agriculture, and medicine. Kluwer Academic/Plenum Publishers, New York, pp 307–340Google Scholar
  77. 77.
    Maheshwari DK, Paul J, Varma A (1994) Paper mill sludge as a potential source for cellulase production by Trichoderma reesei QM 9123 and Aspergillus niger using mixed cultivation. Carbohydr Polym 23:161–163Google Scholar
  78. 78.
    Mandels M, Sternberg D (1976) Recent advances in cellulose technology. J Ferment Technol 54:267–286Google Scholar
  79. 79.
    Mcginn SM, Beauchemin KA, Coates T, Colombatto D (2004) Methane emissions from beef cattle : Effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid. J Anim Sci 82:3346–3356PubMedGoogle Scholar
  80. 80.
    Mienda BS, Idi A, Umar A (2011) Microbiological features of solid state fermentation and its applications—an overview. Res Biotechnol 2:21–26Google Scholar
  81. 81.
    Mischak H, Kubicek CP, Riihr M (1985) Formation and location of glucose oxidase in citric acid producing mycelia of Aspergillus niger. Appl Microbiol Biotechnol 21:27–31Google Scholar
  82. 82.
    Mitchell DA (1992) Growth patters, growth kinetics, and the modeling of growth in solid state cultivation. In: Doelle H, Mitchell DA, Rolz C (eds) Solid substrate cutlivation. Elsevier Science Publishers, Amsterdam, pp 87–112Google Scholar
  83. 83.
    Mitchell DA, Krieger N, Berovic M (2006) Solid-state fermentation bioreactors: fundamentals of design and operation. Springer-Verlag, BerlinGoogle Scholar
  84. 84.
    Mitchell DA, Berovic M, Krieger N (2006) Solid-state fermentation bioreactor fundamentals: Introduction and overview. In: Mitchell DA, Krieger N, Berovic M (eds) Solid-state fermentation bioreactors—fundamentals of design andoperation. Springer-Verlag, Berlin, pp 1–12Google Scholar
  85. 85.
    Miura S, Arimura T, Itoda N et al (2004) Production of L-lactic acid from corncob. J Biosci Bioeng 97:153–157PubMedGoogle Scholar
  86. 86.
    Moresi M, Parente E, Petruccioli M, Federici F (1991) Optimization of fumaric acid production from potato flour by Rhizopus arrhizus. Appl Microbiol Biotechnol 36:35–39Google Scholar
  87. 87.
    Mroweitz U, Christophers E, Altmeyer P (1998) Treatment of psoriasis with fumaric acid esters: results of prospective multicentre study. Br J Dermatol 183:456–460Google Scholar
  88. 88.
    Mukhopadhyay A (2009) Bioconversion of paper mill lignocellulosic materials to lactic acid using cellulase enzyme complex and microbial cultures. Kansas State University, KansasGoogle Scholar
  89. 89.
    Muralidhararao D, Hussain SMDJ, Rangadu VP et al (2007) Fermentatative production of itaconic acid by Aspergillus terreus using Jatropha seed cake. African J Biotechnol 6:2140–2142Google Scholar
  90. 90.
    Netik A, Torres N, Riol J, Kubicek C (1997) Uptake and export of citric acid by Aspergillus niger is reciprocally regulated by manganese ions. Biochim Biophys Acta 1326:287–294PubMedGoogle Scholar
  91. 91.
    Ng T, Hesser R, Stieglitz B et al (1986) Production of tetrahydrofuran/1,4 butanediol by a combined biological and chemical process. Biotechnol Bioeng Symp 17:344–363Google Scholar
  92. 92.
    Nubel R, Ratajak E (1964) Process for producing itaconic acid. United States Patent 3,044,941Google Scholar
  93. 93.
    Okabe M, Lies D, Kanamasa S, Park EY (2009) Biotechnological production of itaconic acid and its biosynthesis in Aspergillus terreus. Appl Microbiol Biotechnol 84:597–606PubMedGoogle Scholar
  94. 94.
    Palmqvist E, Hahn-Hagerdal B (2000) Fermentaion of lignocellulose hydrolysates. I: inhibition and detoxification. Bioresour Technol 74:17–24Google Scholar
  95. 95.
    Pandey A, Selvakumar P, Soccol CR, Nigam P (1999) Solid state fermentation for the production of industrial enzymes. Curr Sci 77:149–162Google Scholar
  96. 96.
    Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84Google Scholar
  97. 97.
    Pandey A, Soccol CR, Larroche C (2008) Introduction. In: Pandey A, Soccol CR, Larroche C (eds) Currentdevelopments insolid-state fermentation. Asiatech Publishers Inc, New Delhi, pp 3–12Google Scholar
  98. 98.
    Pandey A, Soccol CR, Larroche C (2008) Current developments on solid-state fermentation. Asiatech Publishers Inc, New DelhiGoogle Scholar
  99. 99.
    Papagianni M, Mattey M, Berovic M, Kristiansen B (1999) Aspergillus niger morphology and citric acid production in submerged batch fermentation: effects of culture pH, phosphate, and manganese levels. Food Technol Biotechnol 37:165–171Google Scholar
  100. 100.
    Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport, and modeling. Biotechnol Adv 25:244–263PubMedGoogle Scholar
  101. 101.
    Park YS, Kang SW, Lee JS et al (2002) Xylanase production in solid state fermentation by Aspergillus niger mutant using statistical experimental designs. Appl Microbiol Biotechnol 58:761–766PubMedGoogle Scholar
  102. 102.
    Peleg Y, Stieglitz B, Goldberg I (1988) Malic acid accumulation by Aspergillus flavus. I. Biochemical aspects of acid biosynthesis. Appl Microbiol Biotechnol 28:69–75Google Scholar
  103. 103.
    Petruccioli M, Angian E, Federicih F (1996) Semi-continuous fumaric acid production by Rhizopus arrhizus immobilized in polyurethane sponge. Process Biochem 31:463–469Google Scholar
  104. 104.
    Petruccioli M, Pulci V, Federici F (2009) Itaconic acid production by Aspergillus terreus on raw starchy materials. Lett Appl Microbiol 28:309–312Google Scholar
  105. 105.
    Pfeifer VF, Vojnovich C, Heger EN (1952) Itaconic acid by fermentation with Aspergillus terreus. Ind Eng Chem 44:2975–2980Google Scholar
  106. 106.
    Phrueksawan P, Kulpreecha S, Sooksai S, Thongchul N (2012) Direct fermentation of L (+)-lactic acid from cassava pulp by solid state culture of Rhizopus oryzae. Bioprocess Biosyst Eng 35:1429–1436PubMedGoogle Scholar
  107. 107.
    Rahardjo YSP, Tramper J, Rinzema A (2006) Modeling conversion and transport phenomena in solid-state fermentation: a review and perspectives. Biotechnol Adv 24:161–179PubMedGoogle Scholar
  108. 108.
    Reese ET, Mandels M (1966) β-glucanases other than cellulase. Methods Enzymol 8:607–615Google Scholar
  109. 109.
    Rhodes R, Moyer A, Smith ML, Kelley SE (1959) Production of fumaric acid by Rhizopus arrhizus. Appl Microbiol 7:74–80PubMedCentralPubMedGoogle Scholar
  110. 110.
    Rhodes R, Lagoda A, Misenheimer TJ et al (1962) Production of fumaric acid in 20-L fermentors. Appl Microbiol 10:9–15PubMedCentralPubMedGoogle Scholar
  111. 111.
    Riscaldati E, Moresi M, Federici F, Petruccioli M (2000) Direct ammonium fumarate production by Rhizopus arrhizus under phosphorous limitation. Biotechnol Lett 22:1043–1047Google Scholar
  112. 112.
    Roa Engel CA, Straathof AJJ, Zijlmans TW et al (2008) Fumaric acid production by fermentation. Appl Microbiol Biotechnol 78:379–389PubMedCentralPubMedGoogle Scholar
  113. 113.
    Rodríguez-López J, Sánchez AJ, Gómez DM et al (2012) Fermentative production of fumaric acid from Eucalyptus globulus wood hydrolyzates. J Chem Technol Biotechnol 87:1036–1040Google Scholar
  114. 114.
    Romano AH, Bright MM, Scott WE (1967) Mechanism of fumaric acid accumulation in Rhizopus nigricans. J Bacteriol 93:600–604PubMedCentralPubMedGoogle Scholar
  115. 115.
    Ruengruglikit C, Hang Y (2003) L(+)-lactic acid production from corncobs by Rhizopus oryzae NRRL-395. LWT-Food Sci Technol 36:573–575Google Scholar
  116. 116.
    Saito K, Hasa Y, Abe H (2012) Production of lactic acid from xylose and wheat straw by Rhizopus oryzae. J Biosci Bioeng 114:166–169PubMedGoogle Scholar
  117. 117.
    Sato K, Nagatani M, Nakamura K, Sato S (1983) Growth estimation of Candida lipolytica from oxygen uptake in a solid state culture with forced areation. J Ferment Technol 61:623–629Google Scholar
  118. 118.
    Singh K, Sczakas G, Soccol R, Pandey A (2008) Production of enzymes by solid-state fermentation. In: Pandey A, Soccol CR, Larroche C (eds) Current developments in solid-state fermentation. Asiatech Publishers Inc, New Delhi, pp 183–204Google Scholar
  119. 119.
    Singhania RR, Patel AK, Soccol CR, Pandey A (2009) Recent advances in solid-state fermentation. Biochem Eng J 44:13–18Google Scholar
  120. 120.
    Sivan A, Elad Y, Chet I (1984) Biological control effects of a new isolate of Trichoderma harzanium on Pythium aphanidermatum. Phytopathology 74:498–501Google Scholar
  121. 121.
    Soccol CR, Marin B, Raimbault M (1994) Potential of solid-state fermentation for the production of L(+)-lactic acid by Rhizopus oryzae. Appl Microbiol Biotechnol 41:286–290Google Scholar
  122. 122.
    Soccol CR, Vandenberghe LPS, Rodigues C et al (2008) Production of organic acids by solid-state fermentation. In: Pandey A, Soccol CR, Larroche C (eds) Current developments in solid-state fermentation. Asiatech Publishers Inc, New Delhi, pp 205–229Google Scholar
  123. 123.
    Stoilova IS, Gargova SA, Krastanov I (2005) Production of enzymes by mixed culture from mycelial fungi in solid-state fermentation. Biotechnol Biotechnol Equip 19:103–108Google Scholar
  124. 124.
    Takahashi T, Sakaguchi K, Asai T (1925) Studies on the acids formed by Rhizopus species. Bull Agric Chem Soc Japan 5:46–49Google Scholar
  125. 125.
    Terebiznik MR, Pilosof AR (1999) Biomass estimation in solid state fermentation by modeling dry matter weight loss. Biotechnol Tech 13:215–219Google Scholar
  126. 126.
    Tsai YC, Huang MC, Lin SF, Su YC (2001) Method for the production of itaconic acid using Aspergillus terreus solid-state fermentation. United States Patent 6,171,831 B1Google Scholar
  127. 127.
    Tsao GT, Cao NJ, Du J, Gong CS (1999) Production of multifunctional organic acids from renewable resources. In: Scheper T (ed) Advances in biochemical engineering. Springer-Verlag, Berlin, pp 243–280Google Scholar
  128. 128.
    Vandenberghe LPS, Soccol CR, Prado FC, Pandey A (2004) Comparison of citric acid production by solid-state fermentation in flask, column, tray, and drum bioreactors. Appl Biochem Biotechnol 118:293–303PubMedGoogle Scholar
  129. 129.
    Vassilev N, Kautola H, Linko Y-Y (1992) Immobilized Aspergillus terreus in itaconic acid production from glucose. Biotechnol Lett 14:201–206Google Scholar
  130. 130.
    Wang W, Kang L, Lee YY (2010) Production of cellulase from kraft paper mill sludge by Trichoderma reesei rut C-30. Appl Biochem Biotechnol 161:382–394PubMedGoogle Scholar
  131. 131.
    Werpy T, Petersen G, Aden A, et al. (2007) Top value-added chemicals from biomass volume I—results of screening for potential candidates from sugars and synthesis gas. US Department of Energy, Oak Ridge, TN. Available via http://www1.eere.energy.gov/bioenergy/pdfs/35523.pdf. Accessed 5 Feb 2014
  132. 132.
    West TP (2008) Fumaric acid production by Rhizopus oryzae on corn distillers’ grains with solubles. Res J Microbiol 3:35–40Google Scholar
  133. 133.
    West TP (2011) Malic acid production from thin stillage by Aspergillus species. Biotechnol Lett 33:2463–2467PubMedGoogle Scholar
  134. 134.
    Willke T, Vorlop K-D (2001) Biotechnological production of itaconic acid. Appl Microbiol Biotechnol 56:289–295PubMedGoogle Scholar
  135. 135.
    Winskill N (1983) Tricarboxylic acid cycle activity in relation to itaconic acid biosynthesis. J Gen Microbiol 129:2877–2883Google Scholar
  136. 136.
    Wright B, Longacre A, Reimers J (1996) Models of metabolism in Rhizopus oryzae. J Theor Biol 182:453–457PubMedGoogle Scholar
  137. 137.
    Xu Q, Li S, Fu Y et al (2010) Two-stage utilization of corn straw by Rhizopus oryzae for fumaric acid production. Bioresour Technol 101:6262–6264PubMedGoogle Scholar
  138. 138.
    Yahiro K, Shibata S, Jia SR et al (1997) Efficient itaconic acid production from raw corn starch. J Ferment Bioeng 84:375–377Google Scholar
  139. 139.
    Yamamoto K, Tosa T, Yamashita K (1976) Continuous production of L-malic acid by immobilized Brevibacterium ammoniagenescells. Eur J Appl Microbiol 3:169–183Google Scholar
  140. 140.
    Zaldivar J, Nielsen J, Olsson L (2001) Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56:17–34PubMedGoogle Scholar
  141. 141.
    Zhang ZY, Jin B, Kelly JM (2007) Production of lactic acid from renewable materials by Rhizopus fungi. Biochem Eng J 35:251–263Google Scholar
  142. 142.
    Zhang K, Zhang B, Yang ST (2013) Production of citric, itaconic, fumaric, and malic acids in filamentous fungal fermentation. In: Yang ST, El-Enshasy HA, Thongchul N (eds) Bioprocessingtechnologies inbiorefinery for sustainable production offuels, chemicals, and polymers. John Wiley & Sons Inc, Hoboken, pp 375–397Google Scholar
  143. 143.
    Zhou Y (1999) Fumaric acid fermentation by Rhizopus oryzae in submerged systems. Purdue UniversityGoogle Scholar
  144. 144.
    Zhou Y, Du J, Tsao GT (2000) Mycelial pellet formation by Rhizopus oryzae ATCC 20344. Appl Biochem Biotechnol 84–86:779–789PubMedGoogle Scholar
  145. 145.
    Zhou X, Wu Q, Cai Z, Zhang J (2000) Studies on the correlation between production of L-malic acid and some cytosolic enzymes in the L-malic acid producing strain Aspergillus sp. N1-14. Wei Sheng Wu Xue Bao 40:500–506PubMedGoogle Scholar
  146. 146.
    Zhou Y, Du J, Tsao GT (2002) Comparison of fumaric acid production by Rhizopus oryzae using different neutralizing agents. Bioprocess Biosyst Eng 25:179–181PubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology and Biotechnology 2015

Authors and Affiliations

  1. 1.Department of Chemical and Paper EngineeringWestern Michigan UniversityKalamazooUSA

Personalised recommendations