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Applied Microbiology and Biotechnology

, Volume 99, Issue 17, pp 6971–6986 | Cite as

Biotransformations of organic compounds mediated by cultures of Aspergillus niger

  • Igor A. Parshikov
  • Kellie A. Woodling
  • John B. Sutherland
Mini-Review

Abstract

Many different organic compounds may be converted by microbial biotransformation to high-value products for the chemical and pharmaceutical industries. This review summarizes the use of strains of Aspergillus niger, a well-known filamentous fungus used in numerous biotechnological processes, for biochemical transformations of organic compounds. The substrates transformed include monocyclic, bicyclic, and polycyclic aromatic hydrocarbons; azaarenes, epoxides, chlorinated hydrocarbons, and other aliphatic and aromatic compounds. The types of reactions performed by A. niger, although not unique to this species, are extremely diverse. They include hydroxylation, oxidation of various functional groups, reduction of double bonds, demethylation, sulfation, epoxide hydrolysis, dechlorination, ring cleavage, and conjugation. Some of the products may be useful as new investigational drugs or chemical intermediates.

Keywords

Arenes Aspergillus niger Biotransformation Hydrocarbons Organic compounds 

Notes

Acknowledgments

The authors would like to thank Dr. C. E. Cerniglia, Dr. F. A. Beland, Dr. L. Loukotková, and Dr. B. D. Erickson for their helpful comments on the manuscript. The views presented in this article do not necessarily reflect those of the US Food and Drug Administration.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Adelin E, Martin M-T, Bricot M-F, Cortial S, Retailleau P, Ouazzani J (2012) Biotransformation of natural compounds: unexpected thio conjugation of Sch-642305 with 3-mercaptolactate catalyzed by Aspergillus niger ATCC 16404. Phytochemistry 84:135–140CrossRefPubMedGoogle Scholar
  2. Aguirre-Pranzoni CB, Furque GI, Ardanaz CE, Pacciaroni A, Sosa V, Tonn CE, Kurina-Sanz M (2011a) Biotransformation of dihydrocoumarin by Aspergillus niger ATCC 11394. ARKIVOC 7:170–181CrossRefGoogle Scholar
  3. Aguirre-Pranzoni C, Orden AA, Bisogno FR, Aradanaz CE, Tonn CE, Kurina-Sanz M (2011b) Coumarin metabolic routes in Aspergillus spp. Fungal Biol 115:245–252CrossRefPubMedGoogle Scholar
  4. Ali S, Haq I (2010) Production of 3,4-dihydroxy L-phenylalanine by a newly isolated Aspergillus niger and parameter significance analysis by Plackett-Burman design. BMC Biotechnol 10:86(8 p)PubMedCentralCrossRefPubMedGoogle Scholar
  5. Arfmann HA, Abraham WR (1993) Microbial reduction of aromatic carboxylic acids. Z Naturforsch C 48:52–57PubMedGoogle Scholar
  6. Atta-ur-Rahman, Choudhary MI, Shaheen F, Rauf A, Farooq A (1998) Microbial transformation of some bioactive natural products. Nat Prod Lett 12:215–222Google Scholar
  7. Auret BJ, Boyd DR, Henbest HB, Ross S (1968) Stereoselectivity in oxidation of thioethers to sulphoxides in presence of Aspergillus niger. J Chem Soc C Org 18:2371–2374CrossRefGoogle Scholar
  8. Baqueiro-Peña I, Rodríguez-Serrano G, González-Zamora E, Augur C, Loera O, Saucedo-Castañeda G (2010) Biotransformation of ferulic acid to 4-vinylguaiacol by a wild and a diploid strain of Aspergillus niger. Bioresour Technol 101:4721–4724CrossRefPubMedGoogle Scholar
  9. Betiku E, Adesina OA (2013) Statistical approach to the optimization of citric acid production using filamentous fungus Aspergillus niger grown on sweet potato starch hydrolyzate. Biomass Bioenergy 55:350–354CrossRefGoogle Scholar
  10. Bhalerao TS, Puranik PR (2007) Biodegradation of organochlorine pesticide, endosulfan, by a fungal soil isolate, Aspergillus niger. Int Biodeterior Biodegrad 59:315–321CrossRefGoogle Scholar
  11. Boaventura MAD, Lopes RFAP, Takahashi JA (2004) Microorganisms as tools in modern chemistry: the biotransformation of 3-indolylacetonitrile and tryptamine by fungi. Braz J Microbiol 35:345–347CrossRefGoogle Scholar
  12. Bocks SM (1967a) Fungal metabolism—I. The transformations of coumarin, o-coumaric acid and trans-cinnamic acid by Aspergillus niger. Phytochemistry 6:127–130CrossRefGoogle Scholar
  13. Bocks SM (1967b) Fungal metabolism—III. The hydroxylation of anisole, phenoxyacetic acid, phenylacetic acid and benzoic acid by Aspergillus niger. Phytochemistry 6:785–789CrossRefGoogle Scholar
  14. Borges KB, Borges WS, Durán-Patrón R, Pupo MT, Bonato PS, Collado IG (2009) Stereoselective biotransformations using fungi as biocatalysts. Tetrahedron Asymmetry 20:385–397CrossRefGoogle Scholar
  15. Byrde RJW, Harris JF, Woodcock D (1956) Fungal detoxication. The metabolism of ω-(2-naphthyloxy)-n-alkylcarboxylic acids by Aspergillus niger. Biochem J 64:154–160PubMedCentralCrossRefPubMedGoogle Scholar
  16. Byrde RJW, Downing DF, Woodcock D (1959) Fungal detoxication. 4. Metabolism of 2-methoxynaphthalene by Aspergillus niger. Biochem J 72:344–348PubMedCentralCrossRefPubMedGoogle Scholar
  17. Castillo JM, Nogales R, Romero E (2014) Biodegradation of 3,4-dichloroaniline by [fungi] isolated from the preconditioning phase of winery wastes subjected to vermicomposting. J Hazard Mater 267:119–127CrossRefPubMedGoogle Scholar
  18. Cerniglia CE, Sutherland JB (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp. 2079–2110CrossRefGoogle Scholar
  19. Chen L, Shen H, Wei C, Zhu Q (2013) Bioresolution of (R)-glycidyl azide by Aspergillus niger ZJUTZQ208: a new and concise synthon for chiral vicinal amino alcohols. Appl Microbiol Biotechnol 97:2609–2616CrossRefPubMedGoogle Scholar
  20. Choi WJ, Huh EC, Park HJ, Lee EY, Choi CY (1998) Kinetic resolution for optically active epoxides by microbial enantioselective hydrolysis. Biotechnol Tech 12:225–228CrossRefGoogle Scholar
  21. Couto SR, Sanromán MÁ (2006) Application of solid-state fermentation to food industry—a review. J Food Eng 76:291–302CrossRefGoogle Scholar
  22. Deas AHB, Clifford DR (1982) Metabolism of the 1,2,4-triazolylmethane fungicides, triadimefon, triadimenol, and diclobutrazol, by Aspergillus niger (van Tiegh.). Pestic Biochem Physiol 17:120–133CrossRefGoogle Scholar
  23. Esmaeili A, Fazeli S, Moazami N (2012) Microbial transformation of α-naphthol by Aspergillus niger—PTCC 5011. Herba Polon 58:38–46Google Scholar
  24. Faulkner JK, Woodcock D (1961) Fungal detoxication. Part V. Metabolism of o- and p-chlorophenoxyacetic acids by Aspergillus niger. J Chem Soc 1961:5397–5400CrossRefGoogle Scholar
  25. Faulkner JK, Woodcock D (1964) Metabolism of 2,4-dichlorophenoxyacetic acid (‘2,4-D’) by Aspergillus niger van Tiegh. Nature 203:865CrossRefPubMedGoogle Scholar
  26. Goswami A, Totleben MJ, Singh AK, Patel RN (1999) Stereospecific enzymatic hydrolysis of racemic epoxide: a process for making chiral epoxide. Tetrahedron Asymmetry 10:3167–3175CrossRefGoogle Scholar
  27. Gowri PM, Haribabu K, Kishore H, Manjusha O, Buiswas S, Murty USN (2011) Microbial transformation of (+)-heraclenin by Aspergillus niger and evaluation of its antiplasmodial and antimicrobial activities. Curr Sci 100:1706–1711Google Scholar
  28. He A, Rosazza JPN (2003) Microbial transformations of S-naproxen by Aspergillus niger ATCC 9142. Pharmazie 58:420–422PubMedGoogle Scholar
  29. Ibrahim A-R, Abul-Hajj YJ (1990) Microbiological transformation of chromone, chromanone, and ring A hydroxyflavones. J Nat Prod 53:1471–1478CrossRefPubMedGoogle Scholar
  30. Islam A, Ghosh R, Banerjee D, Nath P, Mazumder UK, Ghosal S (2008) Biotransformation of 3-hydroxydibenzo-α-pyrone into 3,8-dihydroxydibenzo-α-pyrone and aminoacyl conjugates by Aspergillus niger isolated from native “shilajit”. Electron J Biotechnol 11:3(8 p)CrossRefGoogle Scholar
  31. Jin H, Li Z-Y (2002) Enantioselective hydrolysis of o-nitrostyrene oxide by whole cells of Aspergillus niger CGMCC 0496. Biosci Biotechnol Biochem 66:1123–1125CrossRefPubMedGoogle Scholar
  32. Jin S, Luo M, Wang W, Zhao CJ, Gu CB, Li CY, Zu YG, Fu YJ, Guan Y (2013) Biotransformation of polydatin to resveratrol in Polygonum cuspidatum roots by highly immobilized edible Aspergillus niger and yeast. Bioresour Technol 136:766–770CrossRefPubMedGoogle Scholar
  33. Kaars Sijpesteijn A, Kaslander J, van der Kerk GJM (1962) On the conversion of sodium dimethyldithiocarbamate into its α-aminobutyric acid derivative by microorganisms. Biochim Biophys Acta 62:587–589CrossRefGoogle Scholar
  34. Kamath AV, Vaidyanathan CS (1990) New pathway for the biodegradation of indole in Aspergillus niger. Appl Environ Microbiol 56:275–280PubMedCentralPubMedGoogle Scholar
  35. Kanaly RA, Kim IS, Hur H-G (2005) Biotransformation of 3-methyl-4-nitrophenol, a main product of the insecticide fenitrothion, by Aspergillus niger. J Agric Food Chem 53:6426–6431CrossRefPubMedGoogle Scholar
  36. Kasahara H, Miyazawa M, Kameoka H (1997) Enantioselective accumulation of (−)-pinoresinol through O-demethylation of (±)-eudesmin by Aspergillus niger. Phytochemistry 44:1479–1482CrossRefPubMedGoogle Scholar
  37. Kiran I, Yildirim HN, Hanson JR, Hitchcock PB (2004) The antifungal activity and biotransformation of diisophorone by the fungus Aspergillus niger. J Chem Technol Biotechnol 79:1366–1370CrossRefGoogle Scholar
  38. Kluyver AJ, van Zijp JCM (1951) The production of homogentisic acid out of phenylacetic acid by Aspergillus niger. Antonie Van Leeuwenhoek 17:315–324CrossRefPubMedGoogle Scholar
  39. Krishna C (2005) Solid-state fermentation systems—an overview. Crit Rev Biotechnol 25:1–30CrossRefPubMedGoogle Scholar
  40. Kurbanoglu EB, Zilbeyaz K, Kurbanoglu NI, Kilic H (2007) Enantioselective reduction of substituted acetophenones by Aspergillus niger. Tetrahedron Asymmetry 18:1159–1162CrossRefGoogle Scholar
  41. Lazarovits G, Hill J, King RR, Calhoun LA (2004) Biotransformation of the Streptomyces scabies phytotoxin thaxtomin A by the fungus Aspergillus niger. Can J Microbiol 50:121–126CrossRefPubMedGoogle Scholar
  42. LeMahieu RA, Tabenkin B, Berger J, Kierstead RW (1970) Microbiological hydroxylation of allethrone. J Org Chem 35:1687–1688CrossRefPubMedGoogle Scholar
  43. Liu SY, Schocken M, Rosazza JPN (1996) Microbial transformations of clomazone. J Agric Food Chem 44:313–319CrossRefGoogle Scholar
  44. Lomascolo A, Lesage-Meessen L, Haon M, Navarro D, Antona C, Faulds C, Marcel A (2001) Evaluation of the potential of Aspergillus niger species for the bioconversion of L-phenylalanine into 2-phenylethanol. World J Microbiol Biotechnol 17:99–102CrossRefGoogle Scholar
  45. Miersch O, Porzel A, Wasternack C (1999) Microbial conversion of jasmonates—hydroxylations by Aspergillus niger. Phytochemistry 50:1147–1152CrossRefPubMedGoogle Scholar
  46. Mikami Y, Fukunaga Y, Arita M, Kisaki T (1981a) Microbial transformation of β-ionone and β-methylionone. Appl Environ Microbiol 41:610–617PubMedCentralPubMedGoogle Scholar
  47. Mikami Y, Fukunaga Y, Arita M, Obi Y, Kisaki T (1981b) Preparation of aroma compounds by microbial transformation of isophorone with Aspergillus niger. Agric Biol Chem 45:791–793CrossRefGoogle Scholar
  48. Myung K, Manthey JA, Narciso JA (2008) Aspergillus niger metabolism of citrus furanocoumarin inhibitors of human cytochrome P450 3A4. Appl Microbiol Biotechnol 78:343–349CrossRefPubMedGoogle Scholar
  49. Noma Y, Asakawa Y (2010) Microbial transformation of (−)-nopol benzyl ether: direct dihydroxylation of benzene ring. Nat Prod Commun 5:1339–1341PubMedGoogle Scholar
  50. Pandey A, Webb C, Soccol CR, Larroche C (eds) (2010) Enzyme technology. Springer, New York, 742 p.Google Scholar
  51. Parshikov IA, Sutherland JB (2014) The use of Aspergillus niger cultures for biotransformation of terpenoids. Proc Biochem 49:2086–2100CrossRefGoogle Scholar
  52. Parshikov IA, Sutherland JB (2015) Biotransformation of steroids and flavonoids by cultures of Aspergillus niger. Appl Biochem Biotechnol. doi: 10.1007/s12010-015-1619-x PubMedGoogle Scholar
  53. Parshikov IA, Modyanova LV, Dovgilivich EV, Terent’ev PB, Vorob’eva LI, Grishina GV (1992) Microbiological transformation of nitrogen-containing heterocyclic compounds. 3. Microbiological synthesis of hydroxy derivatives of 1-benzoylpiperidine and 1-benzoylpyrrolidine. Chem Heterocycl Compd 28:159–162. (Abstract published in 2010 in Cheminform 24) doi:  10.1002/chin.199338068.
  54. Parshikov IA, Freeman JP, Williams AJ, Moody JD, Sutherland JB (1999) Biotransformation of N-acetylphenothiazine by fungi. Appl Microbiol Biotechnol 52:553–557CrossRefPubMedGoogle Scholar
  55. Parshikov IA, Netrusov AI, Sutherland JB (2012) Microbial transformation of azaarenes and potential uses in pharmaceutical synthesis. Appl Microbiol Biotechnol 95:871–889CrossRefPubMedGoogle Scholar
  56. Parshikov IA, Silva EO, Furtado NAJC (2014) Transformation of saturated nitrogen-containing heterocyclic compounds by microorganisms. Appl Microbiol Biotechnol 98:1497–1506CrossRefPubMedGoogle Scholar
  57. Pedragosa-Moreau S, Archelas A, Furstoss R (1993) Microbiological transformations. 28. Enantiocomplementary epoxide hydrolyses as a preparative access to both enantiomers of styrene oxide. J Org Chem 58:5533–5536CrossRefGoogle Scholar
  58. Petta T, Secatto A, Faccioli LH, Moraes LAB (2014) Inhibition of inflammatory response in LPS induced macrophages by 9-KOTE and 13-KOTE produced by biotransformation. Enzym Microb Technol 58:36–43CrossRefGoogle Scholar
  59. Raman TS, Shanmugasundaram ERB (1962) Metabolism of some aromatic acids by Aspergillus niger. J Bacteriol 84:1339–1340PubMedCentralPubMedGoogle Scholar
  60. Ramos AS, Ribeiro JB, Lopes RO, Leite SGF, de Souza ROMA (2011) Highly enantioselective bioreduction of ethyl 3-oxohexanoate. Tetrahedron Lett 52:6127–6129CrossRefGoogle Scholar
  61. Ribeiro JB, de Sousa LMA, Soares MDV, Ramos MDCKV, Neto FRDA, Fraga CAM, Leite SGF, Cordeiro Y, Antunes OAC (2006) Microbial reduction of α-acetyl-γ-butyrolactone. Tetrahedron Asymmetry 17:984–988CrossRefGoogle Scholar
  62. Sack U, Heinze TM, Deck J, Cerniglia CE, Cazau MC, Fritsche W (1997) Novel metabolites in phenanthrene and pyrene transformation by Aspergillus niger. Appl Environ Microbiol 63:2906–2909PubMedCentralPubMedGoogle Scholar
  63. Schuster E, Dunn-Coleman N, Frisvad JC, Van Dijck PWM (2002) On the safety of Aspergillus niger—a review. Appl Microbiol Biotechnol 59:426–435CrossRefPubMedGoogle Scholar
  64. Shahwar D, Raza MA, Ali T, Ahmad VU (2011) Microbial transformation of vanillin isolated from Melia azedarach to vanillyl alcohol followed by protease inhibition and antioxidant activity. J Chem Soc Pak 33:715–719Google Scholar
  65. Shailubhai K, Sahasrabudhe SR, Vora KA, Modi VV (1984) Degradation of chlorinated benzoates by Aspergillus niger. Experientia 40:406–407CrossRefGoogle Scholar
  66. Šnajdrová R, Kristová-Mylerová V, Crestia D, Nikolaou K, Kuzma M, Lemaire M, Gallienne E, Bolte J, Bezouška K, Křen V, Martínková L (2004) Nitrile biotransformation by Aspergillus niger. J Mol Catal B 29:227–232CrossRefGoogle Scholar
  67. Sutherland JB, Freeman JP, Williams AJ, Deck J (1998) Metabolism of cinnoline to N-oxidation products by Cunninghamella elegans and Aspergillus niger. J Ind Microbiol Biotechnol 21:225–227CrossRefGoogle Scholar
  68. Sutherland JB, Heinze TM, Schnackenberg LK, Freeman JP, Williams AJ (2011) Biotransformation of quinazoline and phthalazine by Aspergillus niger. J Biosci Bioeng 111:333–335CrossRefPubMedGoogle Scholar
  69. Takahashi H, Hashimoto T, Noma Y, Asakawa Y (1993) Biotransformation of 6-gingerol and 6-shogaol by Aspergillus niger. Phytochemistry 34:1497–1500CrossRefGoogle Scholar
  70. Torres-Mancera MT, Baqueiro-Peña I, Figueroa-Montero A, Rodríguez-Serrano G, González-Zamora E, Favela-Torres E, Saucedo-Castañeda G (2013) Biotransformation and improved enzymatic extraction of chlorogenic acid from coffee pulp by filamentous fungi. Biotechnol Prog 29:337–345CrossRefPubMedGoogle Scholar
  71. Utkin LM (1950) Gomogentizinovaya kislota v obmene plesnevykh gribov. [Homogentisic acid in the fungus metabolism.]. Biokhimiya 15:330–333Google Scholar
  72. Vorobyeva LI, Parshikov IA, Dorre M, Dovgilevich EV, Modyanova LV, Terentyev PB, Nikishova NG (1990) Microbial transformation of N-containing heterocyclic compounds. II. Hydroxylation of ethylpyridine by microscopic fungi. Biotekhnologiya 4:24–27[In Russian]Google Scholar
  73. Wang Y-L, Wang H, Lu Y-X, Cheng X-C, Han L-L, Yuan S-J, Yang D-X, Zhang Q-L, Wu C-T (2009) Microbial transformation of epothilone A by Aspergillus niger AS 3.739. J Asian Nat Prod Res 11:357–364CrossRefPubMedGoogle Scholar
  74. Woodcock D (1964) Microbial degradation of synthetic compounds. Annu Rev Phytopathol 2:321–340CrossRefGoogle Scholar
  75. Wunder T, Kremer S, Sterner O, Anke H (1994) Metabolism of the polycyclic aromatic hydrocarbon pyrene by Aspergillus niger SK 9317. Appl Microbiol Biotechnol 42:636–641CrossRefPubMedGoogle Scholar
  76. Yadav S, Yadav RSS, Yadava S, Yadav KDS (2011) Stereoselective hydroxylation of ethylbenzene to (R)-1-phenylethanol using mycelia of Aspergillus niger as catalyst. Catal Commun 12:781–784CrossRefGoogle Scholar
  77. Yamazaki Y, Hayashi Y, Arita M, Hieda T, Mikami Y (1988) Microbial conversion of α-ionone, α-methylionone, and α-isomethylionone. Appl Environ Microbiol 54:2354–2360PubMedCentralPubMedGoogle Scholar
  78. Yang R-L, Jia T-L, Zhang R-Q (2005) Microbial transformation of fraxinellone by Aspergillus niger. J Asian Nat Prod Res 7:843–845CrossRefPubMedGoogle Scholar
  79. Yogambal RK, Karegoudar TB (1997) Metabolism of polycyclic aromatic hydrocarbons by Aspergillus niger. Indian J Exp Biol 35:1021–1023PubMedGoogle Scholar
  80. Zheng L, Zheng P, Sun Z, Bai Y, Wang J, Guo X (2007) Production of vanillin from waste residue of rice bran oil by Aspergillus niger and Pycnoporus cinnabarinus. Bioresour Technol 98:1115–1119CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  • Igor A. Parshikov
    • 1
  • Kellie A. Woodling
    • 2
  • John B. Sutherland
    • 3
  1. 1.Institute of Applied MechanicsRussian Academy of SciencesMoscowRussia
  2. 2.Division of Biochemical Toxicology, National Center for Toxicological ResearchU S Food and Drug AdministrationJeffersonUSA
  3. 3.Division of Microbiology, National Center for Toxicological ResearchU S Food and Drug AdministrationJeffersonUSA

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