Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport and modeling.

Citric acid is regarded as a metabolite of energy metabolism, of which the concentration will rise to appreciable amounts only under conditions of substantive metabolic imbalances. Citric acid fermentation conditions were established during the 1930s and 1940s, when the effects of various medium components were evaluated. The biochemical mechanism by which Aspergillus niger accumulates citric acid has continued to attract interest even though its commercial production by fermentation has been established for decades. Although extensive basic biochemical research has been carried out with A. niger, the understanding of the events relevant for citric acid accumulation is not completely understood. This review is focused on citric acid fermentation by A. niger. Emphasis is given to aspects of fermentation biochemistry, membrane transport in A. niger and modeling of the production process.

[1]  M. Papagianni.  Morphology and citric acid production of 'Aspergillus niger' in submerged fermentation. , 1995 .

[2]  M. Wolschek,et al.  Trehalose-6-phosphate synthase A affects citrate accumulation by Aspergillus niger under conditions of high glycolytic flux. , 1996, FEMS microbiology letters.

[3]  C. Kubicek,et al.  An indirect method for studying the fine control of citric acid formation byAspergillus niger , 2005, Biotechnology Letters.

[4]  G. Kontopidis,et al.  Citrate transport during the citric acid fermentation by Aspergillus niger , 1995, Biotechnology Letters.

[5]  K. Kirimura,et al.  Citric acid production by 2-deoxyglucose-resistant mutant strains of Aspergillus niger , 1992, Applied Microbiology and Biotechnology.

[6]  B. Sanwal,et al.  THE ALLOSTERIC NATURE OF NAD-SPECIFIC ISOCITRIC DEHYDROGENASE FROM ASPERGILLI. , 1965, Canadian journal of biochemistry.

[7]  L. Karaffa,et al.  The biochemistry of citric acid accumulation by Aspergillus niger. , 2001, Acta Microbiologica et Immunologica Hungarica.

[8]  Julia M. La Nauze.  Aconitase and isocitric dehydrogenases of Aspergillus niger in relation to citric acid production. , 1966 .

[9]  Brian McNeil,et al.  Dissolved carbon dioxide effects on morphology, growth, and citrate production in Aspergillus niger A60 , 1997 .

[10]  H. Mischak,et al.  Citrate inhibition of glucose uptake in Aspergillus niger , 1984, Biotechnology Letters.

[11]  B. Kristiansen,et al.  Citric Acid Biotechnology , 1998 .

[12]  C. Kubicek,et al.  Partial purification and regulatory properties of phosphofructokinase from Aspergillus niger. , 1983, The Biochemical journal.

[13]  L. Boddy,et al.  Purification and characterisation of an Aspergillus niger invertase and its DNA sequence , 1993, Current Genetics.

[14]  C. Kubicek.  The role of the citric acid cycle in fungal organic acid fermentations. , 1987, Biochemical Society symposium.

[15]  M. Papagianni,et al.  Morphological development of Aspergillus niger in submerged citric acid fermentation as a function of the spore inoculum level. Application of neural network and cluster analysis for characterization of mycelial morphology , 2006, Microbial cell factories.

[16]  E O Voit,et al.  Optimization of nonlinear biotechnological processes with linear programming: Application to citric acid production by Aspergillus niger , 2000, Biotechnology and bioengineering.

[17]  N. Torres,et al.  Modeling approach to control of carbohydrate metabolism during citric acid accumulation by Aspergillus niger: II. Sensitivity analysis , 1994, Biotechnology and bioengineering.

[18]  J. Visser,et al.  Isolation and transformation of the pyruvate kinase gene of Aspergillus nidulans , 1988, Current Genetics.

[19]  M. Legiša,et al.  Glycerol synthesis by Aspergillus niger under citric acid accumulating conditions , 1986 .

[20]  C. Kubicek,et al.  Regulation of citric acid production by oxygen: Effect of dissolved oxygen tension on adenylate levels and respiration in Aspergillus niger , 1980, European journal of applied microbiology and biotechnology.

[21]  K. Kirimura,et al.  Enhancement and repression of cyanide-insensitive respiration in Aspergillus niger. , 1996, FEMS microbiology letters.

[22]  N. Torres,et al.  Uptake and export of citric acid by Aspergillus niger is reciprocally regulated by manganese ions. , 1997, Biochimica et biophysica acta.

[23]  W. Cleland,et al.  Tracer experiments on the mechanism of citric acid formation by Aspergillus niger. , 1954, The Journal of biological chemistry.

[24]  I. Maddox,et al.  Effect of interruptions to the air supply on citric acid production by Aspergillus niger , 1986 .

[25]  John G. Anderson,et al.  Mitochondrial activity during citric acid production by Aspergillus niger , 1972 .

[26]  M. Papagianni,et al.  Modeling the mechanisms of glucose transport through the cell membrane of Aspergillus niger in submerged citric acid fermentation processes , 2004 .

[27]  N. Torres,et al.  Modeling approach to control of carbohydrate metabolism during citric acid accumulation by Aspergillus niger: I. Model definition and stability of the steady state , 1994, Biotechnology and bioengineering.

[28]  B. Kristiansen,et al.  Morphology and citric acid production of Aspergillus niger PM 1 , 1994, Biotechnology Letters.

[29]  C. Kubicek,et al.  Changes in the concentration of fructose 2,6-bisphosphate in Aspergillus niger during stimulation of acidogenesis by elevated sucrose concentration. , 1990, Biochimica et biophysica acta.

[30]  C. Kubicek,et al.  Regulation of citrate synthase from the citric acid-accumulating fungus, Aspergillus niger. , 1980, Biochimica et biophysica acta.

[31]  I. Maddox,et al.  The effect of the sugar source on citric acid production by Aspergillus niger , 1984, Applied Microbiology and Biotechnology.

[32]  S. Ledakowicz,et al.  A kinetic model to predict biomass content for Aspergillus niger germinating spores in the submerged culture , 2006 .

[33]  I. Suzuki,et al.  Pyruvate carboxylase of Aspergillus niger: kinetic study of a biotin-containing carboxylase. , 1969, Canadian journal of biochemistry.

[34]  N. Rao,et al.  Mechanisms of citric acid fermentation by Aspergillus niger , 1984 .

[35]  H. Müller,et al.  Oxalate accumulation from citrate by Aspergillus niger , 1975, Archives of Microbiology.

[36]  B. Kristiansen,et al.  The influence of glucose concentration on citric acid production and morphology of Aspergillus niger in batch and culture , 1999 .

[37]  Y. Peleg,et al.  Localization of pyruvate carboxylase in organic acid-producing Aspergillus strains , 1990, Applied and environmental microbiology.

[38]  M. Papagianni,et al.  Fate and Role of Ammonium Ions during Fermentation of Citric Acid by Aspergillus niger , 2005, Applied and Environmental Microbiology.

[39]  T. Roukas,et al.  The effect of pH on production of citric and gluconic acid from beet molasses using continuous culture , 1988, Biotechnology Letters.

[40]  C. R I S T I A N,et al.  Regulation of Phosphofructokinase from Aspergillus niger : Effect of Fructose 2 , 6-Bisphosphate on the Action of Citrate , Ammonium Ions and AMP , 1986 .

[41]  C. G. Sinclair,et al.  Production of citric acid in continuous culture , 1979 .

[42]  C. Kubicek,et al.  Kinetics of biomass formation and citric acid production by Aspergillus niger on pilot plant scale , 1981 .

[43]  C. Kubicek,et al.  Pyruvate kinase from Aspergillus niger: a regulatory enzyme in glycolysis? , 1984, Canadian journal of microbiology.

[44]  M. Mattey,et al.  Simple diffusion is the primary mechanism for glucose uptake during the production phase of the Aspergillus niger citric acid process. , 2000, Biotechnology and bioengineering.

[45]  Christian P. Kubicek,et al.  The influence of type and concentration of the carbon source on production of citric acid by Aspergillus niger , 1989, Applied Microbiology and Biotechnology.

[46]  M. Mattey.  The production of organic acids. , 1992, Critical reviews in biotechnology.

[47]  C. Lentz,et al.  Submerged citric acid fermentation of sugar beet molasses: effect of pressure and recirculation of oxygen. , 1961, Canadian journal of microbiology.

[48]  H. Weiss,et al.  The role of the proton-pumping and alternative respiratory chain NADH:ubiquinone oxidoreductases in overflow catabolism of Aspergillus niger. , 1993, European journal of biochemistry.

[49]  C. Kubicek,et al.  Characterization and regulatory properties of a single hexokinase from the citric acid accumulating fungus Aspergillus niger. , 1994, Biochimica et biophysica acta.

[50]  Christian P. Kubicek,et al.  Citric Acid Fermentation , 1985 .

[51]  M. C. Rubio,et al.  Purification and characterization of invertase from Aspergillus niger , 1995, Current Microbiology.

[52]  Marvin J. Johnson,et al.  The Interdependence of Medium Constituents in Citric Acid Production by Submerged Fermentation , 1948, Journal of bacteriology.

[53]  Increased citric acid production by mutants of Aspergillus niger with increased glycolytic capacity , 1989 .

[54]  H. Rehm,et al.  Influence of sucrose concentration and phosphate limitation on citric acid production by immobilized cells of Aspergillus niger , 1989, Applied Microbiology and Biotechnology.

[55]  M. J. Johnson,et al.  Effect of the Composition of the Sporulation Medium on Citric Acid Production by Aspergillus niger in Submerged Culture , 1947, Journal of bacteriology.

[56]  S. Nakamura,et al.  Multiple forms of glucose oxidase with different carbohydrate compositions. , 1981, Biochimica et biophysica acta.

[57]  C. Kubicek,et al.  Influence of manganese on enzyme synthesis and citric acid accumulation inAspergillus niger , 1977, European journal of applied microbiology and biotechnology.

[58]  M. J. Johnson,et al.  The pyruvate carboxylase of Aspergillus niger. , 1962, The Journal of biological chemistry.

[59]  C. Kubicek,et al.  Inhibition of citric acid accumulation by manganese ions in Aspergillus niger mutants with reduced citrate control of phosphofructokinase , 1986, Journal of bacteriology.

[60]  K. Kirimura,et al.  Alterations of Respiratory Systems in Aspergillus niger under the Conditions of Citric Acid Fermentation , 1987 .

[61]  C. Kubicek,et al.  Influence of manganese on morphology and cell wall composition of Aspergillus niger during citric acid fermentation , 1980, Archives of Microbiology.

[62]  M. Legiša,et al.  Evidence for the activation of 6-phosphofructo-1-kinase by cAMP-dependent protein kinase in Aspergillus niger. , 1994, FEMS microbiology letters.

[63]  C. Kubicek,et al.  Presence and regulation of the alpha-ketoglutarate dehydrogenase multienzyme complex in the filamentous fungus Aspergillus niger , 1985, Journal of bacteriology.

[64]  P. W. Wilson,et al.  Uptake of C14O2 by Aspergillus niger in the formation of citric acid. , 1951, Archives of biochemistry and biophysics.

[65]  J. K. Gupta,et al.  Effect of sugars, hydrogen ion concentration and ammonium nitrate on the formation of citric acid by Aspergillus niger. , 1976, Acta microbiologica Academiae Scientiarum Hungaricae.

[66]  Michael Schmidt,et al.  Concomitant loss of respiratory chain NADH: ubiquinone reductase (complex I) and citric acid accumulation in Aspergillus niger , 1991, Applied Microbiology and Biotechnology.

[67]  W. Harrer,et al.  NADP-specific isocitrate dehydrogenase from the citric acid-accumulating fungus Aspergillus niger. , 1986, The Biochemical journal.

[68]  J. Visser,et al.  Characterisation of the Aspergillus nidulans frA1 mutant: hexose phosphorylation and apparent lack of involvement of hexokinase in glucose repression. , 1996, FEMS microbiology letters.

[69]  C. G. Sinclair,et al.  Production of citric acid in batch culture , 1978 .

[70]  C. T. Evans,et al.  A comparative study of citrate efflux from mitochondria of oleaginous and non-oleaginous yeasts. , 2005, European journal of biochemistry.

[71]  C. Kubicek,et al.  Phosphofructokinase as a regulatory enzyme in citric acid producing Aspergillus niger , 1979 .

[72]  A. Trinci.  Kinetics of the growth of mycelial pellets of Aspergillus nidulans , 1970, Archiv für Mikrobiologie.

[73]  C. Kubicek,et al.  Evidence for a cytoplasmic pathway of oxalate biosynthesis in Aspergillus niger , 1988, Applied and environmental microbiology.

[74]  A. Moyer.  Effect of Alcohols on the Mycological Production of Citric Acid in Surface and Submerged Culture , 1953, Applied microbiology.

[75]  S. Ledakowicz,et al.  Determination of yield and maintenance coefficients in citric acid production by Aspergillus niger , 1996 .

[76]  Effect of lectins and inhibitors on membrane transport in Aspergillus niger , 1988 .

[77]  A. Leonowicz,et al.  Optimization of glucose oxidase synthesis in submerged cultures of Aspergillus niger G-13 mutant , 1988 .

[78]  H. Mischak,et al.  Formation and location of glucose oxidase in citric acid producing mycelia of Aspergillus niger , 2004, Applied Microbiology and Biotechnology.

[79]  B. Kristiansen,et al.  Hyphal vacuolation and fragmentation in batch and fed-batch culture of Aspergillus niger and its relation to citric acid production , 1999 .

[80]  M. Mattey.  Citrate regulation of citric acid production in Aspergillus niger , 1977 .

[81]  Malate dehydrogenase isoenzymes in Aspergillus niger , 1981 .

[82]  A. Perdih,et al.  Composition of Aspergillus niger mycelium during growth on productive and unproductive substrates , 1992 .

[83]  C. Kubicek,et al.  Intracellular location of enzymes involved in citrate production by Aspergillus niger. , 1991, Canadian journal of microbiology.

[84]  N. Torres,et al.  Glucose transport byAspergillus niger: the low-affinity carrier is only formed during growth on high glucose concentrations , 1996, Applied Microbiology and Biotechnology.

[85]  S. M. Martin.  Citric Acid Production by Submerged Fermentation , 1957 .

[86]  B. Kristiansen,et al.  Citric acid production and morphology of Aspergillus niger as functions of the mixing intensity in a stirred tank and a tubular loop bioreactor , 1998 .

[87]  C. Kubicek,et al.  Alternative respiration of Aspergillus niger , 1980 .

[88]  T. Hanley,et al.  The effects of agitation and aeration on the production of gluconic acid byAspergillus niger , 1995 .

[89]  I. Boag,et al.  Application of fed‐batch culture to citric acid production by Aspergillus niger: The effects of dilution rate and dissolved oxygen tension , 1988, Biotechnology and bioengineering.

[90]  M. Legiša,et al.  Glycerol as an initiator of citric acid accumulation in Aspergillus niger , 1986 .

[91]  Disturbed assemble of the respiratory chain NADH: ubiquinone reductase (complex I) in citric-acid-accumulating Aspergillus niger strain B 60 , 1992, Applied Microbiology and Biotechnology.

[92]  H. Horitsu,et al.  Effect of manganese and other heavy metals on submerged citric acid fermentation of molasses , 1966 .

[93]  J. Visser,et al.  Isolation and characterization of the Aspergillus niger pyruvate kinase gene , 1992, Current Genetics.

[94]  M. J. Johnson,et al.  Carbon dioxide fixation by cell-free extracts of Aspergillus niger. , 1960, The Journal of biological chemistry.

[95]  J. Lowenstein.  Citric Acid Cycle: Control and Compartmentation , 1969 .