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

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Journal of Industrial Microbiology & Biotechnology

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.

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References

  1. Abe S, Furuya A, Saito T, Takayama K (1962) Method of producing L-malic acid by fermentation. United States Patent 3,063,910

  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 76:279–284

    Google Scholar 

  3. Anuradha R, Suresh AK, Venkatesh KV (1999) Simultaneous saccharification and fermentation of starch to lactic acid. Process Biochem 35:367–375

    CAS  Google Scholar 

  4. Baldrian P, Val V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521

    CAS  PubMed  Google Scholar 

  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 27:1108–1116

    Google Scholar 

  6. Bellon-Maurel V, Orliac O, Christen P (2003) Sensors and measurements in solid state fermentation: a review. Process Biochem 38:881–896

    CAS  Google Scholar 

  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 226:689–701

    CAS  PubMed  Google Scholar 

  8. Braun S, Vecht-Lifshitz S (1991) Mycelial morphology and metabolite production. Trends Biotechnol 9:63–68

    Google Scholar 

  9. Bressler E, Braun S (2000) Conversion of citric acid to itaconic acid in a novel liquid membrane bioreactor. J Chem Technol Biotechnol 75:66–72

    CAS  Google Scholar 

  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 45:120–128

    CAS  Google Scholar 

  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 305–322

    Google Scholar 

  12. Brock BJ, Rielbe S, Gold MH (1995) Purification and characterization of 1,4-benzoquinone reductase from the basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 61:3076–3081

    PubMed Central  CAS  PubMed  Google Scholar 

  13. Byrne G, Ward O (1989) Effect of nutrition on pellet formation by Rhizopus arrhizus. Biotechnol Bioeng 33:912–914

    CAS  PubMed  Google Scholar 

  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 33:1488–1495

    PubMed Central  CAS  PubMed  Google Scholar 

  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 62:2926–2931

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Cao N, Du J, Chen C et al (1997) Production of fumaric acid by immobilized Rhizopus using rotary biofilm contactor. Appl Biochem Biotechnol 63–65:387–394

    PubMed  Google Scholar 

  17. Carere CR, Sparling R, Cicek N, Levin DB (2008) Third generation biofuels via direct cellulose fermentation. Int J Mol Sci 9:1342–1360

    PubMed Central  CAS  PubMed  Google Scholar 

  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 68:23–28

    CAS  Google Scholar 

  19. Chahal DS (1985) Solid-state fermentation with Trichoderma reesei for cellulase production. Appl Environ Microbiol 49:205–210

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Corte-Real M, Leao C (1990) Transport of malic acid and other dicarboxylic acids in the yeast Hansenula anomala. Appl Environ Microbiol 56:1109–1113

    PubMed Central  CAS  PubMed  Google Scholar 

  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 17:100–108

    CAS  Google Scholar 

  22. D’Souza J, Volfova O (1982) The Effect of pH on the production of cellulases in Aspergillus terreus. Eur J Appl Microbiol Biotechnol 16:123–125

    Google Scholar 

  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 40:801–807

    CAS  Google Scholar 

  24. Dashtban M, Schraft H, Qin W (2009) Fungal bioconversion of lignocellulosic residues; opportunities & perspectives. Int J Biol Sci 5:578–595

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Deshusses MA (1997) Biological waste air treatment in biofilters. Curr Opin Biotechnol 8:335–339

    CAS  PubMed  Google Scholar 

  26. Du J, Cao N, Gong CS et al (1997) Fumaric acid production in airlift loop reactor with porous sparger. Appl Biochem Biotechnol 63–65:541–556

    PubMed  Google Scholar 

  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 38:1643–1646

    CAS  Google Scholar 

  28. Duenas R, Tengerdy RP, Gutiérrez-Correa M (1995) Cellulase production by mixed fungi in fermentation of bagasse. World J Microbiol Biotechnol 11:333–337

    CAS  PubMed  Google Scholar 

  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 41:2103–2112

    CAS  Google Scholar 

  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 225–261

    Google Scholar 

  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 18:390–398

    CAS  Google Scholar 

  32. Ferreira JA, Lennartsson PR, Edebo L, Taherzadeh MJ (2013) Zygomycetes-based biorefinery: present status and future prospects. Bioresour Technol 135:523–532

    CAS  PubMed  Google Scholar 

  33. Figueiredo Z, Carvalo L Jr (1991) L-malic acid production using immobilized Saccharomyces cerevisiae. Appl Microbiol Biotechnol 30:214–217

    Google Scholar 

  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 30:114–118

    CAS  Google Scholar 

  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 30:227–234

    CAS  Google Scholar 

  36. Foster JW, Waksman SA (1939) The production of fumaric acid by molds belonging to the genus Rhizopus. J Am Chem Soc 61:127–135

    CAS  Google Scholar 

  37. Gangl IC, Weigland WA, Keller FA (1990) Economic comparison of calcium fumarate and sodium fumarate production by Rhizopus arrhizus. Appl Biochem Biotechnol 24–25:663–677

    Google Scholar 

  38. Garg SK, Neelakantan S (1982) Studies on the properties of cellulase enzyme from Aspergillus terreus GN1. Biotechnol Bioeng 24:737–742

    CAS  PubMed  Google Scholar 

  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 33:21–25

    CAS  Google Scholar 

  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 27:1353–1361

    CAS  PubMed  Google Scholar 

  41. Goldberg I, Rokem JS, Pines O (2006) Organic acids: old metabolites, new themes. J Chem Technol Biotechnol 8:1601–1611

    Google Scholar 

  42. Gross R, Rhano K (2002) Biodegradable polymers for the environment. Science 297:803–807

    CAS  PubMed  Google Scholar 

  43. Gutierrez-Correa M, Tengerdy RP (1997) Production of cellulase on sugar cane bagasse by fungal mixed culture solid substrate fermentation. Biotechnol Lett 19:665–667

    CAS  Google Scholar 

  44. Gutierrez-Correa M, Tengerdy RP (1998) Xylanase production by fungal mixed culture solid substrate fermentation on sugar cane bagasse. Biotechnol Lett 20:45–47

    CAS  Google Scholar 

  45. Gyamerah MH (1995) Oxygen requirement and energy relations of itaconic acid fermentation by Aspergillus terreus NRRL 1960. Appl Microbiol Biotechnol 44:20–26

    Google Scholar 

  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 21:265–272

    CAS  Google Scholar 

  47. Henriksson G, Johansson G, Pettersson G (2000) A critical review of cellobiose dehydrogenases. J Biotechnol 78:93–113

    CAS  PubMed  Google Scholar 

  48. Hölker U, Höfer M, Lenz J (2004) Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Appl Microbiol Biotechnol 64:175–186

    PubMed  Google Scholar 

  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 18:358–360

    CAS  Google Scholar 

  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 39–48

  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 23:265–276

    CAS  Google Scholar 

  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 8:2283–2288

    CAS  Google Scholar 

  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 10:4428–4434

    CAS  Google Scholar 

  54. Johnson KG (1990) Exocellular β-mannanases from hemicellulolytic fungi. World J Microbiol Biotechnol 6:209–217

    CAS  PubMed  Google Scholar 

  55. Ju N, Wang SS (1986) Continuous production of itaconic acid by Aspergillus terreus immobilized in a porous disk bioreactor. Appl Microbiol Biotechnol 23:311–314

    CAS  Google Scholar 

  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 41:49–53

    Google Scholar 

  57. Kane J, Finlay A, Amann P (1945) Production of itaconic acid. United States Patent 2,835,283

  58. Kautola H, Vahvaselka M, Linko Y-L, Linko P (1985) Itaconic acid production by immobilized Aspergillus terreus from xylose and glucose. Biotechnol Lett 7:167–172

    CAS  Google Scholar 

  59. Kautola H, Vassilev N, Linko YY (1989) Itaconic acid production by immobilized Aspergillus terreus on surcose medium. Biotechnol Lett 11:313–318

    CAS  Google Scholar 

  60. Kautola H, Linko Y (1989) Fumaric acid production from xylose by immobilized Rhizopus arrhizus cells. Appl Microbiol Biotechnol 31:448–452

    CAS  Google Scholar 

  61. Kautola H (1990) Itaconic acid production from xylose in repeated-batch and continuous bioreactors. Appl Microbiol Biotechnol 33:7–11

    CAS  Google Scholar 

  62. Kenealy W, Zaady E, Preez JC et al (1986) Biochemical aspects of fumaric acid accumulation by Rhizopus arrhizus. Appl Environ Microbiol 52:128–133

    PubMed Central  CAS  PubMed  Google Scholar 

  63. Kennes C, Thalasso F (1998) Waste gas biotreatment technology. J Chem Technol Biotechnol 72:303–319

    CAS  Google Scholar 

  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 5:49–53

    CAS  Google Scholar 

  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 42:381–386

    CAS  Google Scholar 

  66. Kinoshita K (1929) Production of itaconic acid and mannitol by Aspergillus itaconicus. J Chem Soc Japan 50:583–593

    CAS  Google Scholar 

  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

    PubMed Central  PubMed  Google Scholar 

  68. Kubicek C, Karaffa L (2006) Organic acids. In: Ratledge C, Kristiansen B (eds) Basic biotechnology. Cambridge University Press, UK, pp 359–380

    Google Scholar 

  69. Kurzatowski W, Torronen A, Filipek J et al (1996) Glucose-induced secretion of Trichoderma reesei xylanases. Appl Environ Microbiol 62:2859–2865

    Google Scholar 

  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 39:824–827

    CAS  Google Scholar 

  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 99:5859–5866

    CAS  PubMed  Google Scholar 

  72. Ling L, Ng T (1989) Fermentation process for carboxylic acids. United States Patent 4,877,731

  73. Lockwood LB, Ward GE (1945) Fermentation process for itaconic acid. Ind Eng Chem 37:405–406

    CAS  Google Scholar 

  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 53–62

    Google Scholar 

  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 110:2123–2130

    CAS  PubMed  Google Scholar 

  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 307–340

    Google Scholar 

  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 23:161–163

    CAS  Google Scholar 

  78. Mandels M, Sternberg D (1976) Recent advances in cellulose technology. J Ferment Technol 54:267–286

    CAS  Google Scholar 

  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 82:3346–3356

    CAS  PubMed  Google Scholar 

  80. Mienda BS, Idi A, Umar A (2011) Microbiological features of solid state fermentation and its applications—an overview. Res Biotechnol 2:21–26

    Google Scholar 

  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 21:27–31

    CAS  Google Scholar 

  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 87–112

    Google Scholar 

  83. Mitchell DA, Krieger N, Berovic M (2006) Solid-state fermentation bioreactors: fundamentals of design and operation. Springer-Verlag, Berlin

    Google Scholar 

  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 1–12

    Google Scholar 

  85. Miura S, Arimura T, Itoda N et al (2004) Production of L-lactic acid from corncob. J Biosci Bioeng 97:153–157

    CAS  PubMed  Google Scholar 

  86. Moresi M, Parente E, Petruccioli M, Federici F (1991) Optimization of fumaric acid production from potato flour by Rhizopus arrhizus. Appl Microbiol Biotechnol 36:35–39

    CAS  Google Scholar 

  87. Mroweitz U, Christophers E, Altmeyer P (1998) Treatment of psoriasis with fumaric acid esters: results of prospective multicentre study. Br J Dermatol 183:456–460

    Google Scholar 

  88. Mukhopadhyay A (2009) Bioconversion of paper mill lignocellulosic materials to lactic acid using cellulase enzyme complex and microbial cultures. Kansas State University, Kansas

    Google Scholar 

  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 6:2140–2142

    CAS  Google Scholar 

  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 1326:287–294

    CAS  PubMed  Google Scholar 

  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 17:344–363

    Google Scholar 

  92. Nubel R, Ratajak E (1964) Process for producing itaconic acid. United States Patent 3,044,941

  93. Okabe M, Lies D, Kanamasa S, Park EY (2009) Biotechnological production of itaconic acid and its biosynthesis in Aspergillus terreus. Appl Microbiol Biotechnol 84:597–606

    CAS  PubMed  Google Scholar 

  94. Palmqvist E, Hahn-Hagerdal B (2000) Fermentaion of lignocellulose hydrolysates. I: inhibition and detoxification. Bioresour Technol 74:17–24

    CAS  Google Scholar 

  95. Pandey A, Selvakumar P, Soccol CR, Nigam P (1999) Solid state fermentation for the production of industrial enzymes. Curr Sci 77:149–162

    CAS  Google Scholar 

  96. Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84

    CAS  Google Scholar 

  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 3–12

    Google Scholar 

  98. Pandey A, Soccol CR, Larroche C (2008) Current developments on solid-state fermentation. Asiatech Publishers Inc, New Delhi

    Google Scholar 

  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 37:165–171

    CAS  Google Scholar 

  100. Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport, and modeling. Biotechnol Adv 25:244–263

    CAS  PubMed  Google Scholar 

  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 58:761–766

    CAS  PubMed  Google Scholar 

  102. Peleg Y, Stieglitz B, Goldberg I (1988) Malic acid accumulation by Aspergillus flavus. I. Biochemical aspects of acid biosynthesis. Appl Microbiol Biotechnol 28:69–75

    CAS  Google Scholar 

  103. Petruccioli M, Angian E, Federicih F (1996) Semi-continuous fumaric acid production by Rhizopus arrhizus immobilized in polyurethane sponge. Process Biochem 31:463–469

    CAS  Google Scholar 

  104. Petruccioli M, Pulci V, Federici F (2009) Itaconic acid production by Aspergillus terreus on raw starchy materials. Lett Appl Microbiol 28:309–312

    Google Scholar 

  105. Pfeifer VF, Vojnovich C, Heger EN (1952) Itaconic acid by fermentation with Aspergillus terreus. Ind Eng Chem 44:2975–2980

    CAS  Google Scholar 

  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 35:1429–1436

    CAS  PubMed  Google Scholar 

  107. Rahardjo YSP, Tramper J, Rinzema A (2006) Modeling conversion and transport phenomena in solid-state fermentation: a review and perspectives. Biotechnol Adv 24:161–179

    CAS  PubMed  Google Scholar 

  108. Reese ET, Mandels M (1966) β-glucanases other than cellulase. Methods Enzymol 8:607–615

    CAS  Google Scholar 

  109. Rhodes R, Moyer A, Smith ML, Kelley SE (1959) Production of fumaric acid by Rhizopus arrhizus. Appl Microbiol 7:74–80

    PubMed Central  CAS  PubMed  Google Scholar 

  110. Rhodes R, Lagoda A, Misenheimer TJ et al (1962) Production of fumaric acid in 20-L fermentors. Appl Microbiol 10:9–15

    PubMed Central  CAS  PubMed  Google Scholar 

  111. Riscaldati E, Moresi M, Federici F, Petruccioli M (2000) Direct ammonium fumarate production by Rhizopus arrhizus under phosphorous limitation. Biotechnol Lett 22:1043–1047

    CAS  Google Scholar 

  112. Roa Engel CA, Straathof AJJ, Zijlmans TW et al (2008) Fumaric acid production by fermentation. Appl Microbiol Biotechnol 78:379–389

    PubMed Central  CAS  PubMed  Google Scholar 

  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 87:1036–1040

    Google Scholar 

  114. Romano AH, Bright MM, Scott WE (1967) Mechanism of fumaric acid accumulation in Rhizopus nigricans. J Bacteriol 93:600–604

    PubMed Central  CAS  PubMed  Google Scholar 

  115. Ruengruglikit C, Hang Y (2003) L(+)-lactic acid production from corncobs by Rhizopus oryzae NRRL-395. LWT-Food Sci Technol 36:573–575

    CAS  Google Scholar 

  116. Saito K, Hasa Y, Abe H (2012) Production of lactic acid from xylose and wheat straw by Rhizopus oryzae. J Biosci Bioeng 114:166–169

    CAS  PubMed  Google Scholar 

  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 61:623–629

    CAS  Google Scholar 

  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 183–204

    Google Scholar 

  119. Singhania RR, Patel AK, Soccol CR, Pandey A (2009) Recent advances in solid-state fermentation. Biochem Eng J 44:13–18

    CAS  Google Scholar 

  120. Sivan A, Elad Y, Chet I (1984) Biological control effects of a new isolate of Trichoderma harzanium on Pythium aphanidermatum. Phytopathology 74:498–501

    Google Scholar 

  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 41:286–290

    CAS  Google Scholar 

  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 205–229

    Google Scholar 

  123. Stoilova IS, Gargova SA, Krastanov I (2005) Production of enzymes by mixed culture from mycelial fungi in solid-state fermentation. Biotechnol Biotechnol Equip 19:103–108

    CAS  Google Scholar 

  124. Takahashi T, Sakaguchi K, Asai T (1925) Studies on the acids formed by Rhizopus species. Bull Agric Chem Soc Japan 5:46–49

    Google Scholar 

  125. Terebiznik MR, Pilosof AR (1999) Biomass estimation in solid state fermentation by modeling dry matter weight loss. Biotechnol Tech 13:215–219

    CAS  Google Scholar 

  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 B1

  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 243–280

    Google Scholar 

  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 118:293–303

    CAS  PubMed  Google Scholar 

  129. Vassilev N, Kautola H, Linko Y-Y (1992) Immobilized Aspergillus terreus in itaconic acid production from glucose. Biotechnol Lett 14:201–206

    Google Scholar 

  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 161:382–394

    CAS  PubMed  Google Scholar 

  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. West TP (2008) Fumaric acid production by Rhizopus oryzae on corn distillers’ grains with solubles. Res J Microbiol 3:35–40

    CAS  Google Scholar 

  133. West TP (2011) Malic acid production from thin stillage by Aspergillus species. Biotechnol Lett 33:2463–2467

    CAS  PubMed  Google Scholar 

  134. Willke T, Vorlop K-D (2001) Biotechnological production of itaconic acid. Appl Microbiol Biotechnol 56:289–295

    CAS  PubMed  Google Scholar 

  135. Winskill N (1983) Tricarboxylic acid cycle activity in relation to itaconic acid biosynthesis. J Gen Microbiol 129:2877–2883

    CAS  Google Scholar 

  136. Wright B, Longacre A, Reimers J (1996) Models of metabolism in Rhizopus oryzae. J Theor Biol 182:453–457

    CAS  PubMed  Google Scholar 

  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 101:6262–6264

    CAS  PubMed  Google Scholar 

  138. Yahiro K, Shibata S, Jia SR et al (1997) Efficient itaconic acid production from raw corn starch. J Ferment Bioeng 84:375–377

    CAS  Google Scholar 

  139. Yamamoto K, Tosa T, Yamashita K (1976) Continuous production of L-malic acid by immobilized Brevibacterium ammoniagenescells. Eur J Appl Microbiol 3:169–183

    CAS  Google Scholar 

  140. Zaldivar J, Nielsen J, Olsson L (2001) Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56:17–34

    CAS  PubMed  Google Scholar 

  141. Zhang ZY, Jin B, Kelly JM (2007) Production of lactic acid from renewable materials by Rhizopus fungi. Biochem Eng J 35:251–263

  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 375–397

    Google Scholar 

  143. Zhou Y (1999) Fumaric acid fermentation by Rhizopus oryzae in submerged systems. Purdue University

  144. Zhou Y, Du J, Tsao GT (2000) Mycelial pellet formation by Rhizopus oryzae ATCC 20344. Appl Biochem Biotechnol 84–86:779–789

    PubMed  Google Scholar 

  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 40:500–506

    CAS  PubMed  Google Scholar 

  146. Zhou Y, Du J, Tsao GT (2002) Comparison of fumaric acid production by Rhizopus oryzae using different neutralizing agents. Bioprocess Biosyst Eng 25:179–181

    CAS  PubMed  Google Scholar 

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Mondala, A.H. Direct fungal fermentation of lignocellulosic biomass into itaconic, fumaric, and malic acids: current and future prospects. J Ind Microbiol Biotechnol 42, 487–506 (2015). https://doi.org/10.1007/s10295-014-1575-4

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