Skip to main content
Log in

Co-consumption of glucose and xylose for organic acid production by Aspergillus carbonarius cultivated in wheat straw hydrolysate

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Aspergillus carbonarius exhibits excellent abilities to utilize a wide range of carbon sources and to produce various organic acids. In this study, wheat straw hydrolysate containing high concentrations of glucose and xylose was used for organic acid production by A. carbonarius. The results indicated that A. carbonarius efficiently co-consumed glucose and xylose and produced various types of organic acids in hydrolysate adjusted to pH 7. The inhibitor tolerance of A. carbonarius to the hydrolysate at different pH values was investigated and compared using spores and recycled mycelia. This comparison showed a slight difference in the inhibitor tolerance of the spores and the recycled mycelia based on their growth patterns. Moreover, the wild-type and a glucose oxidase deficient (Δgox) mutant were compared for their abilities to produce organic acids using the hydrolysate and a defined medium. The two strains showed a different pattern of organic acid production in the hydrolysate where the Δgox mutant produced more oxalic acid but less citric acid than the wild-type, which was different from the results obtained in the defined medium This study demonstrates the feasibility of using lignocellulosic biomass for the organic acid production by A. carbonarius.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baroi GN, Baumann I, Westermann P, Gavala HN (2015) Butyric acid fermentation from pretreated and hydrolysed wheat straw by an adapted Clostridium tyrobutyricum strain. Microb Biotechnol 8:874–882

    Article  CAS  Google Scholar 

  • Colabardini AC, Ries LNA, Brown NA, Dos Reis TF, Savoldi M, Goldman MHS, Menino JF, Rodrigues F, Goldman GH (2014) Functional characterization of a xylose transporter in Aspergillus nidulans. Biotechnol Biofuels 7:46

    Article  Google Scholar 

  • Darouneh E, Alavi A, Vosoughi M, Arjmand M, Seifkordi A, Rajabi R (2009) Citric acid production: surface culture versus submerged culture. Afr J Microbiol Res 3:541–545

    CAS  Google Scholar 

  • Dionisi D, Anderson JA, Aulenta F, Mccue A, Paton G (2015) The potential of microbial processes for lignocellulosic biomass conversion to ethanol: a review. J Chem Technol Biotechnol 90:366–383

    Article  CAS  Google Scholar 

  • Elkins JG, Raman B, Keller M (2010) Engineered microbial systems for enhanced conversion of lignocellulosic biomass. Curr Opin Biotechnol 21:657–662

    Article  CAS  Google Scholar 

  • Fencl Z, Leopold J (1959) The inhibition of spore germination of the mould Aspergillus niger by acetic acid. Folia Microbiol 4:7–15

    Article  Google Scholar 

  • Ghareib M (1987) Assimilation of galacturonate by Aspergillus carbonarius. Folia Microbiol 32:211–215

    Article  CAS  Google Scholar 

  • Jönsson LJ, Alriksson B, Nilvebrant N- (2013) Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels 6:16

    Article  Google Scholar 

  • Liaud N, Liaud C, Giniés D, Navarro N, Fabre S, Herpoël Crapart I, Gimbert A, Levasseur S, Raouche J, Sigoillot J-C (2014) Exploring fungal biodiversity: organic acid production by 66 strains of filamentous fungi. Fungal Biol Biotechnol 1:1

    Article  Google Scholar 

  • Linde T, Hansen NB, Lübeck M, Lübeck PS (2014) Fermentation in 24-well plates is an efficient screening platform for filamentous fungi. Lett Appl Microbiol 59:224–230

    Article  CAS  Google Scholar 

  • Lu F, Ping K, Wen L, Zhao W, Wang Z, Chu J, Zhuang Y (2015) Enhancing gluconic acid production by controlling the morphology of Aspergillus niger in submerged fermentation. Process Biochem 50:1342–1348

    Article  CAS  Google Scholar 

  • Maddox IS, Spencer K, Greenwood JM, Dawson MW, Brooks JD (1985) Production of citric acid from sugars present in wood hemicellulose using Aspergillus niger and Saccharomycopsis lipolytica. Biotechnol Lett 7:815–818

    Article  CAS  Google Scholar 

  • Magnuson JK, Lasure LL (2004) Organic acid production by filamentous fungi. Adv Fungal Biotechnol Ind Agricult Med 3:307–340

    Article  Google Scholar 

  • Martinez A, Rodriguez ME, Wells ML, York SW, Preston JF, Ingram LO (2001) Detoxification of dilute acid hydrolysates of lignocellulose with lime. Biotechnol Prog 17:287–293

    Article  CAS  Google Scholar 

  • Meng J, Zhou P, Zhang J, Bao J (2014) High titer citric acid fermentation from corn stover hydrolysate by Aspergillus niger. J East China Univ Sci Technol 40:681–683

    CAS  Google Scholar 

  • Millati R, Niklasson C, Taherzadeh MJ (2002) Effect of pH, time and temperature of overliming on detoxification of dilute-acid hydrolyzates for fermentation by Saccharomyces cerevisiae. Process Biochem 38:515–522

    Article  CAS  Google Scholar 

  • Mohamad R, Mohamed M, Suhaili N, Ariff A (2010) Kojic acid: applications and development of fermentation process for production. Biotechnol Mol Biol Rev 5:24–37

    CAS  Google Scholar 

  • Mondala AH (2015) Direct fungal fermentation of lignocellulosic biomass into itaconic, fumaric, and malic acids: current and future prospects. J Ind Microbiol Biotechnol 42:487–506

    Article  CAS  Google Scholar 

  • Nanda S, Azargohar R, Dalai AK, Kozinski JA (2015) An assessment on the sustainability of lignocellulosic biomass for biorefining. Renew Sustain Energy Rev 50:925–941

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pandey A, Soccol CR (1998) Bioconversion of biomass: a case study of ligno-cellulosics bioconversions in solid state fermentation. Braz Arch Biol Technol 41:379–390

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Quevedo-Hidalgo B, Monsalve-Marín F, Narváez-Rincón PC, Pedroza-Rodríguez AM, Velásquez-Lozano ME (2013) Ethanol production by Saccharomyces cerevisiae using lignocellulosic hydrolysate from Chrysanthemum waste degradation. World J Microbiol Biotechnol 29:459–466

    Article  CAS  Google Scholar 

  • Ronne H (1995) Glucose repression in fungi. Trends Genet 11:12–17

    Article  CAS  Google Scholar 

  • Saber WIA, El-Naggar NE, Abdal-Aziz SA (2010) Bioconversion of lignocellulosic wastes into organic acids by cellulolytic rock phosphate-solubilizing fungal isolates grown under solid-state fermentation conditions. Res J Microbiol 5:1–20

    Article  CAS  Google Scholar 

  • Sakai S, Tsuchida Y, Okino S, Ichihashi O, Kawaguchi H, Watanabe T, Inui M, Yukawa H (2007) Effect of lignocellulose-derived inhibitors on growth of and ethanol production by growth-arrested Corynebacterium glutamicum R. Appl Environ Microbiol 73:2349–2353

    Article  CAS  Google Scholar 

  • Show PL, Oladele KO, Siew QY, Aziz Zakry FA, Lan JC-, Ling TC (2015) Overview of citric acid production from Aspergillus niger. Front Life Sci 8(3):271–283

    Article  CAS  Google Scholar 

  • Soo C, Yap W, Hon W, Phang L (2015) Mini review: hydrogen and ethanol co-production from waste materials via microbial fermentation. World J Microbiol Biotechnol 31:1475–1488

    Article  CAS  Google Scholar 

  • Subtil T, Boles E (2012) Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnol Biofuels 5:14

    Article  CAS  Google Scholar 

  • Taniguchi K, Matsudak K, Teramura H, Wale K (1977) Effect of acetic acid on growth of Aspergillus niger. J Fac Sci Hokkaido Univ Ser 5 Bot 10:189–198

    CAS  Google Scholar 

  • Weyda I, Lübeck M, Ahring BK, Lübeck PS (2014) Point mutation of the xylose reductase (XR) gene reduces xylitol accumulation and increases citric acid production in Aspergillus carbonarius. J Ind Microbiol Biotechnol 41:733–739

    Article  CAS  Google Scholar 

  • Xu Q, Li S, Fu Y, Tai C, Huang H (2010) Two-stage utilization of corn straw by Rhizopus oryzae for fumaric acid production. Bioresour Technol 101:6262–6264

    Article  CAS  Google Scholar 

  • Yang L, Lübeck M, Lübeck PS (2014a) Deletion of glucose oxidase changes the pattern of organic acid production in Aspergillus carbonarius. AMB Express 4:54

    Article  Google Scholar 

  • Yang Z, Bai Z, Sun H, Yu Z, Li X, Guo Y, Zhang H (2014b) Biomass pyrolysis liquid to citric acid via 2-step bioconversion. Microb Cell Fact 13:182

    Article  Google Scholar 

  • Yang L, Lübeck M, Lübeck PS (2015) Effects of heterologous expression of phosphoenolpyruvate carboxykinase and phosphoenolpyruvate carboxylase on organic acid production in Aspergillus carbonarius. J Ind Microbiol Biotechnol 42:1533–1545

    Article  CAS  Google Scholar 

  • Zha Y, Westerhuis JA, Muilwijk B, Overkamp KM, Nijmeijer BM, Coulier L, Smilde AK, Punt PJ (2014) Identifying inhibitory compounds in lignocellulosic biomass hydrolysates using an exometabolomics approach. BMC Biotechnol 14:22

    Article  Google Scholar 

Download references

Acknowledgments

Financial support from the Danish Strategic Research Program MycoFuelChem (DSF Grant No. 11-116803) is acknowledged. We thank laboratory technician Gitte Hinz-Berg for HPLC analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter S. Lübeck.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 143 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, L., Lübeck, M., Souroullas, K. et al. Co-consumption of glucose and xylose for organic acid production by Aspergillus carbonarius cultivated in wheat straw hydrolysate. World J Microbiol Biotechnol 32, 57 (2016). https://doi.org/10.1007/s11274-016-2025-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-016-2025-4

Keywords

Navigation