Substrate Inhibition Kinetic Modelling of the Growth of Bacillus sp. Strain Neni-10 on Phenol
DOI:
https://doi.org/10.54987/jebat.v7i2.1051Keywords:
Substrate Inhibition Kinetics, Bioremediation, Phenol, Aiba, Bacillus sp.Abstract
significant portion of the more than 1.5 million tons of sludge waste produced globally for industrial use consists of phenol and phenolic compounds, some of which are released into the environment without adequate safety assessment or control, leading to soil and water pollution. The potential use of phenol as a carbon source by many bacterial species can help mitigate phenol pollution through bioremediation of this hazardous material. This study employs several microbial growth kinetics models that govern the growth rate of a bacterium on phenol, with a focus on the comparative performance of the popular Haldane model alongside other models. The specific maximum growth rate (μₘ) was initially estimated using the no-lag modified logistics model. Among the kinetic models evaluated, the Aiba model exhibited the highest precision and accuracy, as demonstrated by statistical indices, including the lowest MPSD and AICc values, and bias and accuracy factors closest to 1. Despite variability in its parameter estimates, the Aiba model provided a meaningful kinetic description of phenol inhibition at high concentrations. Models such as Monod, Moser, Pamukoglu and Kargi, and Han-Levenspiel showed poor fitting. The maximum reduction rate, half-saturation constant for maximal reduction, and half-inhibition constant were the designated values of the Aiba constants, which were represented by (m, Ks, and Ki) as 1.30±1.40 hr-1 (S.E.), 524.64±753.63 mg/L (S.E.), and 609.78±196.34 mg/L (S.E.), respectively. The results of curve fitting interpolation should not be regarded as the true value. The actual max is defined as the point at which the slope's gradient reaches zero; in this case, it was determined to be 0.295 h-1 at a phenol concentration of 360 mg/L. This study highlights the advantages of employing substrate inhibition models, such as the Aiba and Haldane models, for accurately characterizing microbial growth in the presence of toxic xenobiotics, like phenol, especially for optimizing bioprocesses, such as wastewater treatment.
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 [Internet]. InTech; 2016 [cited 2020 July 17]. Available from: http://www.intechopen.com/books/environmental-health-risk-hazardous-factors-to-living-species/pesticides-environmental-pollution-and-health
Ayeni O. A preliminary assessment of phenol contamination of Isebo River in south-western Nigeria. Greener J Phys Sci. 2014;4(2):30-7.
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 Sept 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.
Kujur RRA, Das SK. Pseudomonas phenolilytica sp. nov., a novel phenol-degrading bacterium. Arch Microbiol. 2022 May 14;204(6):320.
Rusnam, Gusmanizar N, Rahman MF, Yasid NA. Characterization of a Molybdenum-reducing and Phenol-degrading Pseudomonas sp. strain Neni-4 from soils in West Sumatera, Indonesia. Bull Environ Sci Sustain Manag E-ISSN 2716-5353. 2022 July 31;6(1):1-8.
Hanafee N, Salleh NAM, Ahmad SA, Saada WZ, Yusof MT. Characterization of phenol-degrading fungi isolated from industrial waste water in Malaysia. Asia-Pac J Mol Biol Biotechnol. 2019;27(2):35-43.
Aisami A, Yasid NA, Johari WLW, Shukor MY. Estimation of the Q10 value; the temperature coefficient for the growth of Pseudomonas sp. aq5-04 on phenol. Bioremediation Sci Technol Res. 2017 July 31;5(1):24-6.
Szilveszter S, Fikó DR, Máthé I, Felföldi T, Ráduly B. Kinetic characterization of a new phenol degrading Acinetobacter towneri strain isolated from landfill leachate treating bioreactor. World J Microbiol Biotechnol. 2023 Jan 17;39(3):79.
Mousa A. Isolation and Characterization of Phenol degrading Bacteria from Wastewater. Int J Biol Phys Chem Stud. 2023 Sept 10;5:17-24.
Bandi SS, Mallisetty R, Veluru S, Hamzah HT, Poiba VR, Srikanth R. Isolation, identification and optimization of potential phenol degrading bacterial strain P7 using Gen III microlog. AIP Conf Proc. 2023 Sept 13;2764(1):020007.
Sandhyarani R, Mishra S. Isolation and characterization of phenol degrading organism, optimization using doehlert design. Desalination Water Treat. 2019;148:351-62.
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.
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.
Pamukoglu MY, Kargi F. Elimination of Cu(II) toxicity by powdered waste sludge (PWS) addition to an activated sludge unit treating Cu(II) containing synthetic wastewater. J Hazard Mater. 2007 Sept 5;148(1):274-80.
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 [Internet]. 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.
Ezekiel M. The Sampling Variability of Linear and Curvilinear Regressions: A First Approximation to the Reliability of the Results Secured by the Graphic "Successive Approximation" Method. Ann Math Stat. 1930;1(4):275-333.
Hannan EJ, Quinn BG. The Determination of the Order of an Autoregression. J R Stat Soc Ser B Methodol. 1979;41(2):190-5.
Ross T. Indices for performance evaluation of predictive models in food microbiology. J Appl Bacteriol. 1996;81(5):501-8.
Marquardt DW. An Algorithm for Least-Squares Estimation of Nonlinear Parameters. J Soc Ind Appl Math. 1963;11(2):431-41.
Seidel A, Gelbin D. On applying the ideal adsorbed solution theory to multicomponent adsorption equilibria of dissolved organic components on activated carbon. Chem Eng Sci. 1988 Jan 1;43(1):79-88.
Porter JF, McKay G, Choy KH. The prediction of sorption from a binary mixture of acidic dyes using single- and mixed-isotherm variants of the ideal adsorbed solute theory. Chem Eng Sci. 1999;54(24):5863-85.
Akaike H. A New Look at the Statistical Model Identification. IEEE Trans Autom Control. 1974;19(6):716-23.
Burnham KP, Anderson DR. Multimodel inference: Understanding AIC and BIC in model selection. Sociol Methods Res. 2004;33(2):261-304.
Schwarz G. Estimating the Dimension of a Model. Ann Stat. 1978;6(2):461-4.
Motulsky HJ, Ransnas LA. Fitting curves to data using nonlinear regression: a practical and nonmathematical review. FASEB J. 1987;1(5):365-74.
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 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.
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.
Kong JD. Modeling Microbial Dynamics: Effects on Environmental and Human Health [Internet] [PhD Thesis]. [Canada]: University of Alberta; 2017 [cited 2023 Nov 11]. Available from: https://era.library.ualberta.ca/items/0191844e-958e-49fb-bc42-feec802a29ea/view/b06920dd-a80e-427e-b7b9-4aa9433c579e/Kong_Jude_D_201708_PhD.pdf
Mulchandani A, Luong JHT, Groom C. Substrate inhibition kinetics for microbial growth and synthesis of poly-?-hydroxybutyric acid by Alcaligenes eutrophus ATCC 17697. Appl Microbiol Biotechnol. 1989;30(1):11-7.
Yakasai HM, Babandi A, Uba G. Inhibition Kinetics Study of Molybdenum Reduction by Pantoea sp. strain HMY-P4. J Environ Microbiol Toxicol. 2020 Dec 31;8(2):24-9.
Yakasai HM, Babandi A, Manogaran M. Modelling the Kinetics Molybdenum Reduction Rate by Morganella sp. J Environ Microbiol Toxicol. 2020 Dec 31;8(2):18-23.
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.
Othman AR, Rahim MBHA. Modelling the Growth Inhibition Kinetics of Rhodotorula sp. strain MBH23 (KCTC 11960BP) on Acrylamide. Bioremediation Sci Technol Res. 2019 Dec 28;7(2):20-5.
Habibi A, Vahabzadeh F. Degradation of formaldehyde at high concentrations by phenol-adapted Ralstonia eutropha closely related to pink-pigmented facultative methylotrophs. J Environ Sci Health - Part ToxicHazardous Subst Environ Eng. 2013;48(3):279-92.
Monteiro ÁAMG, Boaventura RAR, Rodrigues AE. Phenol biodegradation by Pseudomonas putida DSM 548 in a batch reactor. Biochem Eng J. 2000 Aug 1;6(1):45-9.
?eker ?, Beyenal H, Salih B, Tanyolaç A. Multi-substrate growth kinetics of Pseudomonas putida for phenol removal. Appl Microbiol Biotechnol. 1997;47(5):610-4.
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.
Saravanan P, Pakshirajan K, Saha P. Kinetics of phenol degradation and growth of predominant Pseudomonas species in a simple batch stirred tank reactor. Bulg Chem Commun. 2011;43(4):502-9.
Halmi MIE, Shukor MS, Johari WLW, Shukor MY. Mathematical modeling of the growth kinetics of Bacillus sp. on tannery effluent containing chromate. J Environ Bioremediation Toxicol. 2014;2(1):6-10.
Hasan SA, Jabeen S. Degradation kinetics and pathway of phenol by Pseudomonas and Bacillus species. Biotechnol Biotechnol Equip. 2015;29(1):45-53.
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.
Christen P, Vega A, Casalot L, Simon G, Auria R. Kinetics of aerobic phenol biodegradation by the acidophilic and hyperthermophilic archaeon Sulfolobus solfataricus 98/2. Biochem Eng J. 2012;62:56-61.
Basak B, Bhunia B, Dutta S, Chakraborty S, Dey A. Kinetics of phenol biodegradation at high concentration by a metabolically versatile isolated yeast Candida tropicalis PHB5. Environ Sci Pollut Res. 2014;21(2):1444-54.
Chakraborty B, Ray L, Basu S. Study of phenol biodegradation by an indigenous mixed consortium of bacteria. Indian J Chem Technol. 2015;22(5):227-33.
Heilbuth NM, Linardi VR, Monteiro AS, da RRA, Mimim LA, Santos VL. Estimation of kinetic parameters of phenol degradation by bacteria isolated from activated sludge using a genetic algorithm. J Chem Technol Biotechnol. 2015;90(11):2066-75.
Nandi L, Panigrahi AK, Maitra N, Chattopadhyay AP, Manna SK. Isolation, characterization and growth kinetics of phenol hyper-tolerant bacteria from sewage-fed aquaculture system. J Environ Sci Health Part A. 2020 Mar 20;55(4):333-44.
Basak B, Jeon BH, Kurade MB, Saratale GD, Bhunia B, Chatterjee PK, et al. Biodegradation of high concentration phenol using sugarcane bagasse immobilized Candida tropicalis PHB5 in a packed-bed column reactor. Ecotoxicol Environ Saf. 2019 Sept 30;180:317-25.
Aljbour SH, Khleifat KM, Tarawneh AA, Asasfeh B, Qaralleh H, El-Hasan T, et al. Growth Kinetics and Toxicity of Pseudomonas fredriksbergsis Grown on Phenol as Sole Carbon Source. J Ecol Eng. 2021;22(10):251-63.
Wen Y, Li C, Song X, Yang Y. Biodegradation of phenol by rhodococcus sp. Strain SKC: Characterization and kinetics study. Molecules. 2020;25(16).
Zhao T, Gao Y, Yu T, Zhang Y, Zhang Z, Zhang L, et al. Biodegradation of phenol by a highly tolerant strain Rhodococcus ruber C1: Biochemical characterization and comparative genome analysis. Ecotoxicol Environ Saf. 2021 Jan 15;208:111709.
Mortazavi A, Hassanshahian M, Ali E, Fenjan MN, Alawadi A, Alsalamy A. Isolation and Identification of Phenol-Degrading Bacteria from Iranian Soil and Leaf Samples. Front Biosci-Elite. 2023 Dec 12;15(4):29.
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