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Investigation of the inhibitory effects of furfural and hydroxymethylfurfural on the production of Aspergillus niger inulinase and modeling of the process

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Abstract

Due to the limited natural resources, the tendency toward using agro-industrial wastes as the main substrate in the biotechnological productions has increased. In order to obtain biologically available compounds out of these wastes, various extraction processes need to be applied. However, during these processes, some other inhibitory compounds such as furfural and hydroxymethylfurfural (HMF) also occur. Therefore, evaluation of these inhibitor effects on the biological systems before using these wastes as substrate is crucial for the overall success of the process. This study was undertaken to investigate the effect of various concentrations of furfural and HMF on the Aspergillus niger A42 (ATCC 204,447) inulinase activity, invertase activity, biomass production, and sugar consumption in sucrose-based medium and to model the production outcomes. The results showed that furfural had higher inhibitory effect on the process than HMF at the same concentrations. However, fungi were able to tolerate up to 3 g/l of HMF or 0.5 g/l of furfural in the production medium with minor changes in the yield. The highest inulinase activities were measured as 268.737 and 197.350 U/ml in the presence of 1 g/l of HMF and 0.1 g/l of furfural, respectively. In these conditions, inulinase productions were successfully represented by Baranyi and Weibull models. This study clearly showed that inulinase production with Aspergillus niger A42 can be successfully performed in the presence of a certain amount of furfural and HMF, which indicates the strength of potential usage of lignocellulosic materials as production substrate.

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Data availability

Data available on request from the authors.

Abbreviations

a:

Delay phase transition coefficient A0

A0 :

Lower asymptote (g/l or U/ml)

AF:

Accuracy factor (–)

Am :

Upper asymptote (g/l or U/ml)

ATCC:

American Type Culture Collection

BF:

Bias factor (–)

Bt :

Transition function

d:

Unitless design parameter

e:

Euler number, 2.718 (–)

Eq:

Equation

h0 :

A parameter calculating the initial physiology state of the cells (g/l or U/ml)

HMF:

5-Hydroxymethyl furfural

H t :

Transition function

k:

A parameter governing the rate at which the response variable approaches its potential maximum (–)

MAE:

Mean absolute error

MGM:

Modified Gompertz model

MLM:

Modified logistic model

MMF:

Morgan–Mercer–Flodin

MRM:

Modified Richards model

n:

Number of observations (–)

Q:

Maximum production-consumption rate (g/l/day or U/ml/day)

QIase :

Maximum inulinase production rate (U/ml/day)

QS :

Maximum sugar utilization rate (g/l/day)

QSase :

Maximum invertase-type production rate (U/ml/day)

R2 :

Determination coefficient (–)

RMSE:

Root mean square error

SUY:

Sugar utilization yield (%)

t:

Sampling time (days)

TL :

Time at half of Am (days)

v:

Dimensionless shape parameter (–)

X:

Total dry biomass (g/l)

β:

Growth displacement (–)

δ:

Allometric constant

ΔS:

Substrate consumption (g/l)

λ:

Lag time (days

References

  1. Singh R, Singh R (2017) Inulinases. In: Current developments in biotechnology and bioengineering. Elsevier, pp 423–446

  2. Driouch H, Hänsch R, Wucherpfennig T, Krull R, Wittmann C (2012) Improved enzyme production by bio-pellets of Aspergillus niger: targeted morphology engineering using titanate microparticles. Biotechnol Bioeng 109(2):462–471

    Article  Google Scholar 

  3. Silva-Santisteban BOY, Maugeri Filho F (2005) Agitation, aeration and shear stress as key factors in inulinase production by Kluyveromyces marxianus. Enzyme Microb Technol 36(5–6):717–724

    Article  Google Scholar 

  4. Ilgın M, Germec M, Turhan I (2019) Inulinase production and mathematical modeling from carob extract by using Aspergillus niger. Biotechnology Progress

  5. Germec M, Gürler HN, Ozcan A, Erkan SB, Karahalil E, Turhan I (2020) Medium optimization and kinetic modeling for the production of Aspergillus niger inulinase. Bioprocess and Biosyst Eng 43(2):217–232

  6. Germec M, Turhan I (2019) Evaluation of carbon sources for the production of inulinase by Aspergillus niger A42 and its characterization. Bioprocess Biosyst Eng 42(12):1993–2005

    Article  Google Scholar 

  7. Karahalil E, Germec M, Karaoglan M, Yatmaz E, Coban HB, Inan M, Turhan I (2020) Partial purification and characterization of a recombinant β-mannanase from Aspergillus fumigatus expressed in Aspergillus sojae grown on carob extract. Biomass Convers Biorefinery 10(4):1189–1205

    Article  Google Scholar 

  8. Germec M, Turhan I (2021) Effect of pH control and aeration on inulinase production from sugarbeet molasses in a bench-scale bioreactor. Biomass Convers Biorefinery:1–13

  9. Gürler HN, Germec M, Turhan I (2020) The inhibition effect of phenol on the production of Aspergillus niger inulinase and its modeling. J Food Process Preserv 45(8):e14522

  10. Galbe M, Wallberg O (2019) Pretreatment for biorefineries: a review of common methods for efficient utilisation of lignocellulosic materials. Biotechnology for Biofuels 12(1):1–26

  11. Almeida JR, Modig T, Petersson A, Hähn-Hägerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol: Int Res Process, Environ Clean Technol 82(4):340–349

    Article  Google Scholar 

  12. Erkan SB, Yatmaz E, Germec M, Turhan I (2020) Effect of furfural concentration on ethanol production using Saccharomyces cerevisiae in an immobilized cells stirred‐tank bioreactor with glucose‐based medium and mathematical modeling. J Food Process Preserv 45(8):e14635

  13. Malav MK, Prasad S, Kharia SK, Kumar S, Sheetal K, Kannojiya S (2017) Furfural and 5-HMF: potent fermentation inhibitors and their removal techniques. Int J Curr Microbiol Appl Sci 6:2060–2066

    Article  Google Scholar 

  14. Lin R, Cheng J, Ding L, Song W, Zhou J, Cen K (2015) Inhibitory effects of furan derivatives and phenolic compounds on dark hydrogen fermentation. Biores Technol 196:250–255

    Article  Google Scholar 

  15. Anburajan P, Pugazhendhi A, Park J-H, Kumar G, Choi C-S, Kim S-H (2017) Inhibitory effect of 5-hydroxymethylfurfural on continuous hydrogen fermentation by mixed culture in a fixed bed reactor. Int J Hydrogen Energy 42(45):27570–27576

    Article  Google Scholar 

  16. Zwietering M, Jongenburger I, Rombouts F, Van’t Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56(6):1875–1881

    Article  Google Scholar 

  17. Stannard C, Williams A, Gibbs P (1985) Temperature/growth relationships for psychrotrophic food-spoilage bacteria. Food Microbiol 2(2):115–122

    Article  Google Scholar 

  18. Weibull W (1951) Wide applicability. J appl mech 103(730):293–297

    Article  MATH  Google Scholar 

  19. Morgan PH, Mercer LP, Flodin NW (1975) General model for nutritional responses of higher organisms. Proc Natl Acad Sci 72(11):4327–4331

    Article  Google Scholar 

  20. Dantigny P, Nanguy SP-M, Judet-Correia D, Bensoussan M (2011) A new model for germination of fungi. Int J Food Microbiol 146(2):176–181

    Article  Google Scholar 

  21. Baranyi J, Roberts TA (1994) A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 23(3–4):277–294

    Article  Google Scholar 

  22. Huang L (2013) Optimization of a new mathematical model for bacterial growth. Food Control 32(1):283–288

    Article  Google Scholar 

  23. Fitzhugh H Jr (1976) Analysis of growth curves and strategies for altering their shape. J Anim Sci 42(4):1036–1051

    Article  Google Scholar 

  24. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426–428. https://doi.org/10.1021/ac60147a030

    Article  Google Scholar 

  25. Zhang H, Zhang J, Bao J (2016) High titer gluconic acid fermentation by Aspergillus niger from dry dilute acid pretreated corn stover without detoxification. Biores Technol 203:211–219

    Article  Google Scholar 

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Acknowledgements

The first author was supported by TUBITAK (The Scientific and Research Council of Turkey) National Scholarship Program for MSc Students. This work was supported by the Akdeniz University Research Foundation (Grant number #FYL-2019-4755).

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Authors and Affiliations

  1. Department of Food Engineering, Akdeniz University, Antalya, 07058, Turkey

    Hilal Nur Gürler & Irfan Turhan

  2. Izmir International Biomedicine and Genome Institute, Dokuz Eylul University, Balcova, Izmir, 35340, Turkey

    Hasan Bugra Coban

Authors
  1. Hilal Nur Gürler
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  2. Hasan Bugra Coban
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  3. Irfan Turhan
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Contributions

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

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Correspondence to Irfan Turhan.

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Gürler, H.N., Coban, H.B. & Turhan, I. Investigation of the inhibitory effects of furfural and hydroxymethylfurfural on the production of Aspergillus niger inulinase and modeling of the process. Biomass Conv. Bioref. 13, 4291–4303 (2023). https://doi.org/10.1007/s13399-022-02440-1

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