Skip to main content
SpringerLink
Log in

Differential Activation of Ferulic Acid Catabolic Pathways of Amycolatopsis sp. ATCC 39116 in Submerged and Surface Cultures

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Amycolatopsis sp. ATCC 39116 catabolizes ferulic acid by the non-oxidative deacetylation and β-oxidation pathways to produce vanillin and vanillic acid, respectively. In submerged culture, vanillin productivity decreased more than 8-fold, when ferulic, p-coumaric, and caffeic acids were employed in pre-cultures of the microorganism in order to activate the ferulic acid catabolic pathways, resulting in a carbon redistribution since vanillic acid and guaiacol productivities increased more than 5-fold compared with control. In contrast, in surface culture, the effects of ferulic and sinapic acids in pre-cultures were totally opposite to those of the submerged culture, directing the carbon distribution into vanillin formation. In surface culture, more than 30% of ferulic acid can be used as carbon source for other metabolic processes, such as ATP regeneration. In this way, the intracellular ATP concentration remained constant during the biotransformation process by surface culture (100 μg ATP/mg protein), demonstrating a high energetic state, which can maintain active the non-oxidative deacetylation pathway. In contrast, in submerged culture, it decreased 3.15-fold at the end of the biotransformation compared with the initial content, showing a low energetic state, while the NAD+/NADH ratio (23.15) increased 1.81-fold. It seems that in submerged culture, low energetic and high oxidative states are the physiological conditions that can redirect the ferulic catabolism into β-oxidative pathway and/or vanillin oxidation to produce vanillic acid.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Sutherland, J. B., Crawford, D. L., & Pometto III, A. L. (1983). Metabolism of cinnamic, p-coumaric, and ferulic acids by Streptomyces setonii. Canadian Journal of Microbiology, 29(10), 1253–1257.

    PubMed  CAS  Google Scholar 

  2. Brown, M. E., Walker, M. C., Nakashige, T. G., Iavarone, A. T., & Chang, M. C. (2011). Discovery and characterization of heme enzymes from unsequenced bacteria: application to microbial lignin degradation. Journal of the American Chemical Society, 133(45), 18006–18009.

    PubMed  CAS  Google Scholar 

  3. Kaur, B., & Chakraborty, D. (2013). Biotechnological and molecular approaches for vanillin production: a review. Applied Biochemistry and Biotechnology, 169(4), 1353–1372.

    PubMed  CAS  Google Scholar 

  4. Asaff, A., & Reyes, Y. (2018) Method and system for the integral treatment of wastewater from the maize industry. US Patent 10,011,509 B2.

  5. Meyer, F., Netzer, J., Meinert, C., Voigt, B., Riedel, K., & Steinbüchel, A. (2018). A proteomic analysis of ferulic acid metabolism in Amycolatopsis sp. ATCC 39116. Applied Microbiology and Biotechnology, 102(14), 6119–6142.

    PubMed  CAS  Google Scholar 

  6. Gallage, N. J., & Møller, B. L. (2015). Vanillin–bioconversion and bioengineering of the most popular plant flavor and its de novo biosynthesis in the vanilla orchid. Molecular Plant, 8(1), 40–57.

    PubMed  CAS  Google Scholar 

  7. Fleige, C., Hansen, G., Kroll, J., & Steinbüchel, A. (2013). Investigation of the Amycolatopsis sp. strain ATCC 39116 vanillin dehydrogenase and its impact on the biotechnical production of vanillin. Applied and Environmental Microbiology, 79(1), 81–90.

    PubMed  PubMed Central  CAS  Google Scholar 

  8. Cai, R., Yuan, Y., Wang, Z., Guo, C., Liu, B., Liu, L., & Yue, T. (2015). Precursors and metabolic pathway for guaiacol production by Alicyclobacillus acidoterrestris. International Journal of Food Microbiology, 214, 48–53.

    PubMed  CAS  Google Scholar 

  9. Johnson, C. W., & Beckham, G. T. (2015). Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin. Metabolic Engineering, 28, 240–247.

    PubMed  CAS  Google Scholar 

  10. Kallscheuer, N., Vogt, M., Kappelmann, J., Krumbach, K., Noack, S., Bott, M., & Marienhagen, J. (2016). Identification of the phd gene cluster responsible for phenylpropanoid utilization in Corynebacterium glutamicum. Applied Microbiology and Biotechnology, 100(4), 1871–1881.

    PubMed  CAS  Google Scholar 

  11. Kasai, D., Kamimura, N., Tani, K., Umeda, S., Abe, T., Fukuda, M., & Masai, E. (2012). Characterization of FerC, a MarR-type transcriptional regulator, involved in transcriptional regulation of the ferulate catabolic operon in Sphingobium sp. strain SYK-6. FEMS Microbiology Letters, 332, 68–75.

    PubMed  CAS  Google Scholar 

  12. Ma, X. K., & Daugulis, A. J. (2014). Effect of bioconversion conditions on vanillin production by Amycolatopsis sp. ATCC 39116 through an analysis of competing by-product formation. Bioprocess and Biosystems Engineering, 37, 891–899.

    PubMed  CAS  Google Scholar 

  13. Asaff, A., De La Torre, M., Mir, A. B., & Ochoa, R. M. M. (2011) Process of production of vanillin with immobilized microorganisms. U.S. patent 2011/0065156A1.

  14. González-Segura, L., Velasco-García, R., & Muñoz-Clares, R. A. (2002). Modulation of the reactivity of the essential cysteine residue of betaine aldehyde dehydrogenase from Pseudomonas aeruginosa. The Biochemical Journal, 361(3), 577–585.

    PubMed  PubMed Central  Google Scholar 

  15. AOAC. (2000). Official methods of analysis. Official method 986.35 (16th ed.). Gaithersburg: Association of Official Analytical Chemists.

    Google Scholar 

  16. Preciado-Saldaña, A. M., Abraham Domínguez-Avila, J., Fernando Ayala-Zavala, J., Villegas-Ochoa, M. A., Sáyago-Ayerdi, S. G., Wall-Medrano, A., & González-Aguilar, G. A. (2019). Formulation and characterization of an optimized functional beverage from hibiscus (Hibiscus sabdariffa L.) and green tea (Camellia sinensis L.). Food Science and Technology International, 25, 547–561.

    PubMed  Google Scholar 

  17. Ou, B., Hampsch-Woodill, M., & Prior, R. L. (2001). Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe. Journal of Agricultural and Food Chemistry, 49(10), 4619–4626.

    PubMed  CAS  Google Scholar 

  18. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254.

    PubMed  CAS  Google Scholar 

  19. Fleige, C., Meyer, F., & Steinbüchel, A. (2016). Metabolic engineering of the actinomycete Amycolatopsis sp. strain ATCC 39116 towards enhanced production of natural vanillin. Applied and Environmental Microbiology, 82(11), 3410–3419.

    PubMed  PubMed Central  CAS  Google Scholar 

  20. Martínez-Cuesta, M., Payne, J., Hanniffy, S. B., Gasson, M. J., & Narbad, A. (2005). Functional analysis of the vanillin pathway in a vdh-negative mutant strain of Pseudomonas fluorescens AN103. Enzyme and Microbial Technology, 37(1), 131–138.

    Google Scholar 

  21. Civolani, C., Barghini, P., Roncetti, A. R., Ruzzi, M., & Schiesser, A. (2000). Bioconversion of ferulic acid into vanillic acid by means of a vanillate-negative mutant of Pseudomonas fluorescens strain BF13. Applied and Environmental Microbiology, 66(6), 2311–2317.

    PubMed  PubMed Central  CAS  Google Scholar 

  22. Achterholt, S., Priefert, H., & Steinbüchel, A. (2000). Identification of Amycolatopsis sp. strain HR167 genes, involved in the bioconversion of ferulic acid to vanillin. Applied Microbiology and Biotechnology, 54(6), 799–807.

    PubMed  CAS  Google Scholar 

  23. Crawford, R. L., & Olson, P. P. (1978). Microbial catabolism of vanillate: decarboxylation to guaiacol. Applied and Environmental Microbiology, 36(4), 539–543.

    PubMed  PubMed Central  CAS  Google Scholar 

  24. Chow, K. T., Pope, M. K., & Davies, J. (1999). Characterization of a vanillic acid non-oxidative decarboxylation gene cluster from Streptomyces sp. D7. Microbiology., 145(9), 2393–2403.

    PubMed  CAS  Google Scholar 

  25. Aguilar, C. N., Augur, C., Favela-Torres, E., & Viniegra-González, G. (2001). Induction and repression patterns of fungal tannase in solid-state and submerged cultures. Process Biochemistry, 36(6), 565–570.

    CAS  Google Scholar 

  26. Renovato, J., Gutiérrez-Sánchez, G., Rodríguez-Durán, L. V., Bergman, C., Rodríguez, R., & Aguilar, C. N. (2011). Differential properties of Aspergillus niger tannase produced under solid-state and submerged fermentations. Applied Biochemistry and Biotechnology, 165(1), 382–395.

    PubMed  CAS  Google Scholar 

  27. Hernández-Domínguez, E. M., Rios-Latorre, R. A., Álvarez-Cervantes, J., Loera-Corral, O., Román-Gutiérrez, A. D., Díaz-Godínez, G., & Mercado-Flores, Y. (2014). Xylanases, cellulases, and acid protease produced by Stenocarpella maydis grown in solid-state and submerged fermentation. BioResources, 9, 2341–2358.

    Google Scholar 

  28. Barrios-González, J., Baños, J. G., Covarrubias, A. A., & Garay-Arroyo, A. (2008). Lovastatin biosynthetic genes of Aspergillus terreus are expressed differentially in solid-state and in liquid submerged fermentation. Applied Microbiology and Biotechnology, 79(2), 179–186.

    PubMed  Google Scholar 

  29. te Biesebeke, R., van Biezen, N., De Vos, W. M., Van Den Hondel, C. A. M. J. J., & Punt, P. J. (2005). Different control mechanisms regulate glucoamylase and protease gene transcription in Aspergillus oryzae in solid-state and submerged fermentation. Applied Microbiology and Biotechnology, 67(1), 75–82.

    Google Scholar 

  30. Otani, H., Stogios, P. J., Xu, X., Nocek, B., Li, S. N., Savchenko, A., & Eltis, L. D. (2015). The activity of CouR, a MarR family transcriptional regulator, is modulated through a novel molecular mechanism. Nucleic Acids Research, 44, 595–607.

    PubMed  PubMed Central  Google Scholar 

  31. Davis, J. R., Goodwin, L. A., Woyke, T., Teshima, H., Bruce, D., Detter, C., & Nolan, M. (2012). Genome sequence of Amycolatopsis sp. strain ATCC 39116, a plant biomass-degrading actinomycete. Journal of Bacteriology, 194(9), 2396–2397.

    PubMed  PubMed Central  CAS  Google Scholar 

  32. Wilkinson, S. P., & Grove, A. (2006). Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Current Issues in Molecular Biology, 8, 51–62.

    PubMed  Google Scholar 

  33. Parke, D., & Ornston, L. N. (2003). Hydroxycinnamate (hca) catabolic genes from Acinetobacter sp. strain ADP1 are repressed by HcaR and are induced by hydroxycinnamoyl-coenzyme a thioesters. Applied and Environmental Microbiology, 69(9), 5398–5409.

    PubMed  PubMed Central  CAS  Google Scholar 

  34. Grove, A. (2013). MarR family transcription factors. Current Biology, 23(4), R142–R143.

    PubMed  CAS  Google Scholar 

  35. Aoki, R., Takeda, T., Omata, T., Ihara, K., & Fujita, Y. (2012). MarR-type transcriptional regulator ChlR activates expression of tetrapyrrole biosynthesis genes in response to low-oxygen conditions in cyanobacteria. The Journal of Biological Chemistry, 287(16), 13500–13507.

    PubMed  PubMed Central  CAS  Google Scholar 

  36. Fuangthong, M., & Helman, J. D. (2002). The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proceedings of the National Academy of Sciences of the United States of America, 99(10), 6690–6695.

    PubMed  PubMed Central  CAS  Google Scholar 

  37. Panmanee, W., Vattanaviboon, P., Poole, L. B., & Mongkolsuk, S. (2006). Novel organic hydroperoxide-sensing and responding mechanisms for OhrR, a major bacterial sensor and regulator of organic hydroperoxide stress. Journal of Bacteriology, 188(4), 1389–1395.

    PubMed  PubMed Central  CAS  Google Scholar 

  38. Miranda, R. U., Gómez-Quiroz, L. E., Mejía, A., & Barrios-González, J. (2013). Oxidative state in idiophase links reactive oxygen species (ROS) and lovastatin biosynthesis: differences and similarities in submerged-and solid-state fermentations. Fungal Biology, 117(2), 85–93.

    PubMed  CAS  Google Scholar 

  39. Miranda, R. U., Gómez-Quiroz, L. E., Mendoza, M., Pérez-Sánchez, A., Fierro, F., & Barrios-González, J. (2014). Reactive oxygen species regulate lovastatin biosynthesis in Aspergillus terreus during submerged and solid-state fermentations. Fungal Biology, 118(12), 979–989.

    PubMed  CAS  Google Scholar 

  40. Perera, I. C., & Grove, A. (2010). Molecular mechanisms of ligand-mediated attenuation of DNA binding by MarR family transcriptional regulators. Journal of Molecular Cell Biology, 2(5), 243–254.

    PubMed  CAS  Google Scholar 

  41. Otani, H., Lee, Y. E., Casabon, I., & Eltis, L. D. (2014). Characterization of p-hydroxycinnamate catabolism in a soil Actinobacterium. Journal of Bacteriology, 196(24), 4293–4303.

    PubMed  PubMed Central  Google Scholar 

  42. Mallinson, S. J., Machovina, M. M., Silveira, R. L., Garcia-Borràs, M., Gallup, N., Johnson, C. W., & Houk, K. N. (2018). A promiscuous cytochrome P450 aromatic O-demethylase for lignin bioconversion. Nature Communications, 9, 1–12.

    CAS  Google Scholar 

  43. Romero-Gómez, S. J., Augur, C., & Viniegra-González, G. (2000). Invertase production by Aspergillus niger in submerged and solid-state fermentation. Biotechnology Letters, 22(15), 1255–1258.

    Google Scholar 

  44. Asaff, A., Cerda-García-Rojas, C. M., Viniegra-González, G., & de la Torre, M. (2006). Carbon distribution and redirection of metabolism in Paecilomyces fumosoroseus during solid-state and liquid fermentations. Process Biochemistry, 41(6), 1303–1310.

    CAS  Google Scholar 

  45. Lima-Pérez, J., López-Pérez, M., Viniegra-González, G., & Loera, O. (2019). Solid-state fermentation of Bacillus thuringiensis var kurstaki HD-73 maintains higher biomass and spore yields as compared to submerged fermentation using the same media. Bioprocess and Biosystems Engineering, 42, 1–9.

    Google Scholar 

  46. Garcia-Ochoa, F., Gomez, E., Santos, V. E., & Merchuk, J. C. (2010). Oxygen uptake rate in microbial processes: an overview. Biochemical Engineering Journal, 49(3), 289–307.

    CAS  Google Scholar 

  47. Jouhten, P., Rintala, E., Huuskonen, A., Tamminen, A., Toivari, M., Wiebe, M., & Maaheimo, H. (2008). Oxygen dependence of metabolic fluxes and energy generation of Saccharomyces cerevisiae CEN. PK113-1A. BMC Systems Biology, 2(1), 60.

    PubMed  PubMed Central  Google Scholar 

  48. Fuchs, G., Boll, M., & Heider, J. (2011). Microbial degradation of aromatic compounds—From one strategy to four. Nature Reviews. Microbiology, 9(11), 803–816.

    PubMed  CAS  Google Scholar 

  49. Akram, M. (2014). Citric acid cycle and role of its intermediates in metabolism. Cell Biochemistry and Biophysics, 68(3), 475–478.

    PubMed  CAS  Google Scholar 

  50. De Graef, M. R., Alexeeva, S., Snoep, J. L., & de Mattos, M. J. T. (1999). The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. Journal of Bacteriology, 181(8), 2351–2357.

    PubMed  PubMed Central  Google Scholar 

  51. Friedrich, T. (1998). The NADH: ubiquinone oxidoreductase (complex I) from Escherichia coli. Biochimica et Biophysica Acta - Bioenergetics, 1364(2), 134–146.

    CAS  Google Scholar 

  52. Du, C., Yan, H., Zhang, Y., Li, Y., & Cao, Z. A. (2006). Use of oxidoreduction potential as an indicator to regulate 1, 3-propanediol fermentation by Klebsiella pneumoniae. Applied Microbiology and Biotechnology, 69(5), 554–563.

    PubMed  CAS  Google Scholar 

  53. Simon, O., Klaiber, I., Huber, A., & Pfannstiel, J. (2014). Comprehensive proteome analysis of the response of Pseudomonas putida KT2440 to the flavor compound vanillin. Journal of Proteomics, 109, 212–227.

    PubMed  CAS  Google Scholar 

  54. Coitinho, J. B., Pereira, M. S., Costa, D. M., Guimarães, S. L., Araújo, S. S., Hengge, A. C., & Nagem, R. A. (2016). Structural and kinetic properties of the aldehyde dehydrogenase NahF, a broad substrate specificity enzyme for aldehyde oxidation. Biochemistry., 55(38), 5453–5463.

    PubMed  CAS  Google Scholar 

  55. Karala, A. R., & Ruddock, L. W. (2007). Does s-methyl methanethiosulfonate trap the thiol–disulfide state of proteins? Antioxidants & Redox Signaling, 9(4), 527–531.

    CAS  Google Scholar 

  56. Velasco-García, R., Zaldívar-Machorro, V. J., Mújica-Jiménez, C., González-Segura, L., & Muñoz-Clares, R. A. (2006). Disulfiram irreversibly aggregates betaine aldehyde dehydrogenase—A potential target for antimicrobial agents against Pseudomonas aeruginosa. Biochemical and Biophysical Research Communications, 341(2), 408–415.

    PubMed  Google Scholar 

  57. Kim, J. J. P., & Miura, R. (2004). Acyl-CoA dehydrogenases and acyl-CoA oxidases: structural basis for mechanistic similarities and differences. European Journal of Biochemistry, 271(3), 483–493.

    PubMed  CAS  Google Scholar 

  58. Amari, D. T., Marques, C. N., & Davies, D. G. (2013). The putative enoyl-CoA hydratase DspI is required for production of the Pseudomonas aeruginosa biofilm bispersion autoinducer, cis-2-decenoic acid. Journal of Bacteriology, 95, 4600–4610.

    Google Scholar 

Download references

Acknowledgments

V. Contreras-Jácquez is thankful to the (CONACYT) scholarship awarded and to Mónica A. Villegas-Ochoa for her helpful assistance.

Funding

This work is financially supported by the Mexican Council of Science and Technology (CONACyT), grant no. 2017-01-6267.

Author information

Authors and Affiliations

  1. Centro de Investigación en Alimentación y Desarrollo, A.C. (Coordinación de Ciencia de los Alimentos), Carretera Gustavo Enrique Astiazarán Rosas 46, La Victoria, CP, 83304, Hermosillo, Sonora, Mexico

    Victor Contreras-Jácquez, Elisa M. Valenzuela-Soto & Ali Asaff-Torres

  2. Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, A.C. (Unidad de Biotecnología Industrial), Camino el Arenero 1227, El Bajío del Arenal, CP, 45019, Zapopan, Jalisco, Mexico

    Jorge Rodríguez-González & Juan Carlos Mateos-Díaz

Authors
  1. Victor Contreras-Jácquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Rodríguez-González
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan Carlos Mateos-Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisa M. Valenzuela-Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ali Asaff-Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Victor Contreras-Jácquez. The first draft of the manuscript was written by Victor Contreras-Jácquez, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ali Asaff-Torres.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(DOCX 556 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Contreras-Jácquez, V., Rodríguez-González, J., Mateos-Díaz, J.C. et al. Differential Activation of Ferulic Acid Catabolic Pathways of Amycolatopsis sp. ATCC 39116 in Submerged and Surface Cultures. Appl Biochem Biotechnol 192, 494–516 (2020). https://doi.org/10.1007/s12010-020-03336-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-020-03336-4

Keywords

Search

Navigation