Substrate Inhibition Kinetics Models for Fitting the Growth Rate of Phenol by an Immobilized Pseudomonas putida

Authors

  • Garba Uba Department of Science Laboratory Technology, College of Science and Technology, Jigawa State Polytechnic, Dutse, PMB 7040, Nigeria.
  • Hafeez Muhammad Yakasai Department of Biochemistry, Faculty of Basic Medical Sciences, College of Health Sciences, Bayero University Kano, Nigeria.
  • Aisami Abubakar Department of Biochemistry, Faculty of Science, Gombe State University, P.M.B 127, Tudun Wada, Gombe, Gombe State, Nigeria.

DOI:

https://doi.org/10.54987/jemat.v10i2.770

Keywords:

Substrate Inhibition Kinetics, phenol, Pseudomonas putida, Immobilized bacterium, Teissier

Abstract

Phenol, in particular, is one of several dangerous synthetic compounds created by humans. There were more than 80,000 chemicals produced in the US for industrial use, and many of these are phenol and phenolic compounds that end up in the environment without being subjected to adequate safety assessment. There are several types of bacteria that may use phenol as a carbon source, making bioremediation of this dangerous material a promising possibility. We found that at very high concentrations of phenol, the growth rate of Pseudomonas putida NAUN-16 was significantly slowed down. The primary growth model modified Gompertz was utilized to obtain the growth parameter specific growth rate. In this study, we continue the work by further modelling the effect of substrate or phenol on the growth rate of the bacterium using several substrate inhibition kinetic models such as Monod, Haldane, Teissier, Aiba, Yano and Koga, Han and Levenspiel, Luong, Moser, Webb and Hinshelwood. The resultant fittings show appreciable fitting with the exception of the Monod model. The Teissier model, as opposed to the more widely used Haldane model, better suited the growth rate data at different concentrations of phenol as judged by the results of the RMSE, AICc, adjustedR2, F-test, and bias and accuracy factor. The designated values of the Teissier constants were maximal reduction rate, half saturation constant for maximal reduction and half inhibition constant which are symbolized by max, Ks and Ki were 0.150 1/hr (95% confidence interval 0.120 to 0.180), 162.19 mg/L (95% C.I.55.58 to 268.79) and 1291.94 mg/L (95% C.I. 1067.24 to 1516.65), respectively. The value generated from curve fitting interpolation should not be taken as the actual value and it should be warned of this as the true mumax should be where the gradient for the slope is zero and in this case the value was approximately 0.097 1/h at 385 mg/L phenol.

References

Özkara A, Akyil D, Konuk M. Pesticides, Environmental Pollution, and Health. In: Larramendy M, Soloneski S, editors. Environmental Health Risk - Hazardous Factors to Living Species. InTech; 2016 2020.

VanDoren PM. The Effects of Exposure to "Synthetic" Chemicals on Human Health: A Review. Risk Anal . 1996;16(3):367-76.

Ayeni O. A preliminary assessment of phenol contamination of Isebo River in south-western Nigeria. Greener J Phys Sci. 2014;4(2):30-7.

Agarry SE, Solomon BO. Kinetics of batch microbial degradation of phenols by indigenous Pseudomonas fluorescence. Int J Environ Sci Technol. 2008;5(2):223-32.

Agarry S e., Durojaiye A o., Yusuf R o., Aremu M o., Solomon B o., Mojeed O. Biodegradation of phenol in refinery wastewater by pure cultures of Pseudomonas aeruginosa NCIB 950 and Pseudomonas fluorescence NCIB 3756. Int J Environ Pollut. 2008 Jan;32(1):3-11.

Agarry SE, Solomon BO, Layokun SK. Substrate inhibition kinetics of phenol degradation by binary mixed culture of Pseudomonas aeruginosa and Pseudomonas fluorescence from steady state and wash- out data. Afr J Biotechnol. 2008;7(21):3927-33.

Agarry SE, Audu TOK, Solomon BO. Substrate inhibition kinetics of phenol degradation by Pseudomonas fluorescence from steady state and wash-out data. Int J Environ Sci Technol. 2009;6(3):443-50.

Bruce RM, Santodonato J, Neal MW. Summary Review of the Health Effects Associated With Phenol. Toxicol Ind Health. 1987 Oct 1;3(4):535-68.

Strikwold M, Spenkelink B, Woutersen RA, Rietjens IMCM, Punt A. Combining in vitro embryotoxicity data with physiologically based kinetic (PBK) modelling to define in vivo dose-response curves for developmental toxicity of phenol in rat and human. Arch Toxicol. 2013 Sep 1;87(9):1709-23.

Kottuparambil S, Kim YJ, Choi H, Kim MS, Park A, Park J, et al. A rapid phenol toxicity test based on photosynthesis and movement of the freshwater flagellate, Euglena agilis Carter. Aquat Toxicol. 2014 Oct 1;155:9-14.

Mohanta VL, Mishra BK. Occurrence and fate of phenolic compounds in groundwater and their associated risks. In: Legacy, Pathogenic and Emerging Contaminants in the Environment. CRC Press; 2021.

Kim JS, Chin P. Acute and chronic toxicity of phenol to mysid, Archaeomysis kokuboi. Korean J Fish Aquat Sci. 1995;28(1):87-97.

Abd Gami A, Shukor A, Yunus M, Abdul Khalil K, Dahalan FA, Khalid A, et al. Phenol and phenolic compounds toxicity. J Environ Microbiol Toxicol. 2014;2(1):11-23.

Gami AA, Shukor MY, Khalil KA, Dahalan FA, Khalid A, Ahmad SA. Phenol and its toxicity. J Environ Microbiol Toxicol. 2014;2(1):11-23.

Dhatwalia VK, Nanda M. Biodegradation of phenol: Mechanisms and applications. Toxicity and Waste Management Using Bioremediation. 2015. 198-214 p.

Duan W, Meng F, Cui H, Lin Y, Wang G, Wu J. Ecotoxicity of phenol and cresols to aquatic organisms: A review. Ecotoxicol Environ Saf. 2018;157:441-56.

US EPA R 05. Human Health Noncarcinogen Fact Sheet for Phenol: (Human Health Noncarcinogen - fish ingestion only), Wisconsin Department of Natural Resources . 2015

Kiviharju K, Salonen K, Leisola M, Eerikäinen T. Modeling and simulation of Streptomyces peucetius var. caesius N47 cultivation and ?-rhodomycinone production with kinetic equations and neural networks. J Biotechnol. 2006;126(3):365-73.

Shokrollahzadeh S, Bonakdarpour B, Vahabzadeh F, Sanati M. Growth kinetics and Pho84 phosphate transporter activity of Saccharomyces cerevisiae under phosphate-limited conditions. J Ind Microbiol Biotechnol. 2007;34(1):17-25.

Arif NM, Ahmad SA, Syed MA, Shukor MY. Isolation and characterization of a phenol-degrading Rhodococcus sp. strain AQ5NOL 2 KCTC 11961BP. J Basic Microbiol. 2013;53(1):9-19.

Hamitouche AE, Bendjama Z, Amrane A, Kaouah F, Hamane D. Relevance of the Luong model to describe the biodegradation of phenol by mixed culture in a batch reactor. Ann Microbiol. 2012;62(2):581-6.

Nickzad A, Mogharei A, Monazzami A, Jamshidian H, Vahabzadeh F. Biodegradation of phenol by Ralstonia eutropha in a Kissiris-immobilized cell bioreactor. Water Environ Res. 2012;84(8):626-34.

Saravanan P, Pakshirajan K, Saha P. Batch growth kinetics of an indigenous mixed microbial culture utilizing m-cresol as the sole carbon source. J Hazard Mater. 2009;162(1):476-81.

Uba G, Yakasai HM, Abubakar A. Mathematical modeling of the biodegradation of phenol from industrial effluents using immobilized Pseudomonas putida. J Biochem Microbiol Biotechnol. 2020 Jul 31;8(1):15-8.

Singh U, Arora NK, Sachan P. Simultaneous biodegradation of phenol and cyanide present in coke-oven effluent using immobilized Pseudomonas putida and Pseudomonas stutzeri. Braz J Microbiol. 2018 Jan 1;49(1):38-44.

Rohatgi A. WebPlotDigitizer. http://arohatgi.info/WebPlotDigitizer/app/ Accessed June 2 2014.; 2015.

Halmi MIE, Shukor MS, Johari WLW, Shukor MY. Modeling the growth curves of Acinetobacter sp. strain DRY12 grown on diesel. J Environ Bioremediation Toxicol. 2014;2(1):33-7.

Khare KS, Phelan Jr FR. Quantitative comparison of atomistic simulations with experiment for a cross-linked epoxy: A specific volume-cooling rate analysis. Macromolecules. 2018;51(2):564-75.

Monod J. The Growth of Bacterial Cultures. Annu Rev Microbiol. 1949;3(1):371-94.

Boon B, Laudelout H. Kinetics of nitrite oxidation by Nitrobacter winogradskyi. Biochem J. 1962;85:440-7.

Teissier G. Growth of bacterial populations and the available substrate concentration. Rev Sci Instrum. 1942;3208:209-14.

Aiba S, Shoda M, Nagatani M. Kinetics of product inhibition in alcohol fermentation. Biotechnol Bioeng. 1968 Nov 1;10(6):845-64.

Yano T, Koga S. Dynamic behavior of the chemostat subject to substrate inhibition. Biotechnol Bioeng. 1969 Mar 1;11(2):139-53.

Han K, Levenspiel O. Extended Monod kinetics for substrate, product, and cell inhibition. Biotechnol Bioeng. 1988;32(4):430-7.

Luong JHT. Generalization of monod kinetics for analysis of growth data with substrate inhibition. Biotechnol Bioeng. 1987;29(2):242-8.

Moser A. Kinetics of batch fermentations. In: Rehm HJ, Reed G, editors. Biotechnology. VCH Verlagsgesellschaft mbH, Weinheim; 1985. p. 243-83.

Webb JLeyden. Enzyme and metabolic inhibitors . New York: Academic Press; 1963. 984 p. Available from: https://www.biodiversitylibrary.org/bibliography/7320

Hinshelwood CN. The chemical kinetics of the bacterial cell. Clarendon Press, Gloucestershire, UK; 1946.

Wayman M, Tseng MC. Inhibition?threshold substrate concentrations. Biotechnol Bioeng. 1976;18(3):383-7.

G?uszcz P, Petera J, Ledakowicz S. Mathematical modeling of the integrated process of mercury bioremediation in the industrial bioreactor. Bioprocess Biosyst Eng. 2011;34(3):275-85.

Kass RE, Raftery AE. Bayes Factors. J Am Stat Assoc. 1995 Jun 1;90(430):773-95.

Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Science & Business Media; 2002. 528 p.

Fritz H, Reineke W, Schmidt E. Toxicity of chlorobenzene on Pseudomonas sp. strain RHO1, a chlorobenzene-degrading strain. Biodegradation. 1991;2(3):165-70.

Saravanan P, Pakshirajan K, Saha P. Kinetics of phenol and m-cresol biodegradation by an indigenous mixed microbial culture isolated from a sewage treatment plant. J Environ Sci. 2008;20(12):1508-13.

Li L, Hong Q, Yan X, Fang G, Ali SW, Li S. Isolation of a malachite green-degrading Pseudomonas sp. MDB-1 strain and cloning of the tmr2 gene. Biodegradation. 2009;20(6):769-76.

Pathak H, Madamwar D. Biosynthesis of indigo dye by newly isolated naphthalene-degrading strain Pseudomonas sp. HOB1 and its application in dyeing cotton fabric. Appl Biochem Biotechnol. 2010;160(6):1616-26.

Hu J, Zhang LL, Chen JM, Liu Y. Degradation of paracetamol by Pseudomonas aeruginosa strain HJ1012. J Environ Sci Health - Part ToxicHazardous Subst Environ Eng. 2013;48(7):791-9.

Wang GL, Li XF, Zhang H, Xiong MH, Li F. Optimization of CTN-4 to chlorothalonil-degrading conditions and a kinetics model. Zhongguo Huanjing KexueChina Environ Sci. 2013;33(11):1999-2005.

Tiong B, Bahari ZM, Irwan SL, Jaafar J, Ibrahim Z, Shahir S. Cyanide degradation by Pseudomonas pseudoalcaligenes strain W2 isolated from mining effluent. Sains Malays. 2015;44(2):233-8.

Vignesh R, Arularasan A, V G, Deepika C. Isolation identification and characterization of potential oil degrading bacteria from oil contaminated sites. 2016 Jan 1;

Zhang C, Wang B, Dai X, Li S, Lu G, Zhou Y. Structure and function of the bacterial communities during rhizoremediation of hexachlorobenzene in constructed wetlands. Environ Sci Pollut Res. 2017 Apr 1;24(12):11483-92.

Habib S, Iruthayam A, Abd Shukor MY, Alias SA, Smykla J, Yasid NA. Biodeterioration of Untreated Polypropylene Microplastic Particles by Antarctic Bacteria. Polymers. 2020 Nov;12(11):2616.

Shettima H, Allamin IA, Halima N, Ismail HY, Musa Y. Isolation and Characterization of Hydrocarbon-degrading Bacteria in Soils of Mechanical Workshops in Maiduguri, Borno State. J Environ Bioremediation Toxicol. 2021 Dec 31;4(2):35-8.

Sufyan AJ, Ibrahim S, Babandi A, Yakasai HM. Characterization of Butachlor Degradation by A Molybdenum-Reducing and Aniline-degrading Pseudomonas sp. J Environ Microbiol Toxicol. 2021 Dec 31;9(2):8-12.

Saravanan P, Pakshirajan K, Saha P. Growth kinetics of an indigenous mixed microbial consortium during phenol degradation in a batch reactor. Bioresour Technol. 2008;99(1):205-9.

Kotturi G, Robinson CW, Inniss WE. Phenol degradation by a psychrotrophic strain of Pseudomonas putida. Appl Microbiol Biotechnol. 1991;34(4):539-43.

Bai J, Wen JP, Li HM, Jiang Y. Kinetic modeling of growth and biodegradation of phenol and m-cresol using Alcaligenes faecalis. Process Biochem. 2007;42(4):510-7.

Long TR, Zhang Z, Zhuan RX. Biodegradation of phenol by a novel isolated bacterium Pseudomonas sp. CN-6. Tumu Jianzhu Yu Huanjing Gongcheng Journal Civ Archit Environ Eng. 2010;32(5):82-7.

Liu J, Wang Q, Yan J, Qin X, Li L, Xu W, et al. Isolation and characterization of a novel phenol degrading bacterial strain WUST-C1. Ind Eng Chem Res. 2013;52(1):258-65.

Basak SP, Sarkar P, Pal P. Isolation and characterization of phenol utilizing bacteria from industrial effluent-contaminated soil and kinetic evaluation of their biodegradation potential. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2014;49(1):67-77.

Ding C, Wang Z, Cai W, Zhou Q, Zhou J. Biodegradation of phenol with Candida tropicalis isolated from aerobic granules. Fresenius Environ Bull. 2014;23(3 A):887-95.

Mohanty SS, Jena HM. Biodegradation of phenol by free and immobilized cells of a novel Pseudomonas sp. nbm11. Braz J Chem Eng. 2017 Mar;34:75-84.

Kiviharju K, Salonen K, Leisola M, Eerikäinen T. Modeling and simulation of Streptomyces peucetius var. caesius N47 cultivation and ?-rhodomycinone production with kinetic equations and neural networks. J Biotechnol. 2006;126(3):365-73.

Agarry SE, Solomon BO. Kinetics of batch microbial degradation of phenols by indigenous Pseudomonas fluorescence. Int J Environ Sci Technol. 2008;5(2):223-32.

Annuar MSM, Tan IKP, Ibrahim S, Ramachandran KB. A kinetic model for growth and biosynthesis of medium-chain-length poly-(3-hydroxyalkanoates) in Pseudomonas putida. Braz J Chem Eng. 2008 Jun;25(2):217-28.

Singh RK, Kumar S, Kumar S, Kumar A. Biodegradation kinetic studies for the removal of p-cresol from wastewater using Gliomastix indicus MTCC 3869. Biochem Eng J. 2008;40(2):293-303.

Sack ELW, van der Wielen PWJJ, van der Kooij D. Flavobacterium johnsoniae as a model organism for characterizing biopolymer utilization in oligotrophic freshwater environments. Appl Environ Microbiol. 2011;77(19):6931-8.

del Barrio MC, Demafelis RB, Mercado SM, Movillon JL, Rebancos CM. Growth kinetics of Rhizopus chinensis Saito BIOTECH 3273 in the production of microbial rennet using coconut paring cake as substrate. Philipp Agric Sci Philipp . 2012 [cited 2020 Dec 20]; Available from: https://agris.fao.org/agris-search/search.do?recordID=PH2014000116

Tavassoli T, Mousavi SM, Shojaosadati SA, Salehizadeh H. Asphaltene biodegradation using microorganisms isolated from oil samples. Fuel. 2012 Mar 1;93:142-8.

Gharibzahedi SMT, Razavi SH, Mousavi M. Kinetic analysis and mathematical modeling of cell growth and canthaxanthin biosynthesis by Dietzia natronolimnaea HS-1 on waste molasses hydrolysate. RSC Adv. 2013;3(45):23495-502.

Vijayalakshmi V, Senthilkumar P, Mophin-Kani K, Sivamani S, Sivarajasekar N, Vasantharaj S. Bio-degradation of Bisphenol A by Pseudomonas aeruginosa PAb1 isolated from effluent of thermal paper industry: Kinetic modeling and process optimization. J Radiat Res Appl Sci. 2018 Jan 1;11(1):56-65.

Zhao H, Zhu J, Liu S, Zhou X. Kinetics study of nicosulfuron degradation by a Pseudomonas nitroreducens strain NSA02. Biodegradation. 2018;29(3):271-83.

Uba G, Abubakar A, Ibrahim S. Optimization of Process Conditions for Effective Degradation of Azo Blue Dye by Streptomyces sp. DJP15: A Secondary Modelling Approac. Bull Environ Sci Sustain Manag. 2021 Dec 31;5(2):28-32.

Najim AA, Ismail ZZ, Hummadi KK. Immobilization of mixed bacteria by novel biocarriers extracted from Cress and Chia seeds for biotreatment of anionic surfactant (SDS)-bearing real wastewaters. Prep Biochem Biotechnol. 2022;

Begum SS, Radha KV. Investigating the performance of inverse fluidized bed biofilm reactor for phenol biodegradation using Pseudomonas fluorescence. In: Proceedings of the International Conference on Green Technology and Environmental Conservation, GTEC-2011. 2011. p. 130-6.

Halmi MIE, Shukor MS, Johari WLW, Shukor MY. Mathematical modelling of the degradation kinetics of Bacillus cereus grown on phenol. J Environ Bioremediation Toxicol. 2014;2(1):1-5.

Downloads

Published

31.12.2022

How to Cite

Uba, G., Yakasai, H. M., & Abubakar, A. (2022). Substrate Inhibition Kinetics Models for Fitting the Growth Rate of Phenol by an Immobilized Pseudomonas putida. Journal of Environmental Microbiology and Toxicology, 10(2), 27–33. https://doi.org/10.54987/jemat.v10i2.770

Issue

Section

Articles