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Phenol biodegradation by plant growth promoting bacterium, S. odorifera: kinetic modeling and process optimization

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Abstract

One of the main organic pollutants that could result from industrial products and chemical transformations is phenol. In the current study, the kinetics of Serratia odorifera, which was isolated from arable soil, was studied by growing it on broth minimal medium spiked with phenol as only carbon source and energy. The newly isolated plant growth-promoting bacterium (PGPB), S. odorifera, was used for the first time for phenol biodegradation. The growth kinetics parameters (phenol-dependent) including maximum specific growth rate (μmax), half-saturation coefficient (Ks), and the Haldane’s growth kinetics inhibition coefficient (Ki), were tested via Haldane inhibition model and resulted on the 0.469 (h −1), 26.6 (mgL−1), and 292 (mgL−1), respectively. The sum of squared error (SSR) of 4.89 × 10–3 was fitted to the experimental data by Haldane equation. The results of phenol biodegradation were fitted into the modified Gombertz model. The increase of phenol concentrations led to increases in both the rate of phenol biodegradation and lagging time. The optimal phenol biodegradation and bacterial growth obtained by S. odorifera, were at 28 °C incubation temperature and a pH of 7.0. The pathway of phenol biodegradation by S. odorifera was proposed in the current study to provide a new insight into synchronization of phenol biodegradation and plant growth-promoting bacteria. This may play an important role in remediation of phenol-contaminated soil besides promoting the plant growth, thus lessening the plant stress.

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References

  • Abboud MM, Khleifat KM, Batarseh M, Tarawneh KA, Al-Mustafa A, Al-Madadhah M (2007) Different optimization conditions required for enhancing the biodegradation of linear alkylbenzosulfonate and sodium dodecyl sulfate surfactants by novel consortium of Acinetobacter calcoaceticus and Pantoea agglomerans. Enzyme Microb Technol 41(4):432–439

    CAS  Google Scholar 

  • Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886. https://doi.org/10.1139/w08-081

    Article  CAS  PubMed  Google Scholar 

  • Agarwal GK, Ghoshal AK (2008) Packed bed dynamics during microbial treatment of wastewater: Modelling and simulation. Bioresour Technol 99:3765–3773

    CAS  PubMed  Google Scholar 

  • Ahmad SA, Shamaan NA, Syed MA, Dahalan FA, Khalil KA, Ab Rahman NA, Shukor MY (2017) Phenol degradation by Acinetobacter sp. in the presence of heavy metals. J Natl Sci Found Sri Lanka 45(3):247–253

    CAS  Google Scholar 

  • Aisami A, Yasid NA, Abd Shukor MY (2020) Optimization of Cultural and physical parameters for phenol biodegradation by newly identified Pseudomonas sp. AQ5–04. J Trop Life Sci 10(3):223–233

    Google Scholar 

  • Al-Asoufi A, Khlaifat A, Tarawneh A, Alsharafa K, Al-Limoun M, Khleifat K (2017) Bacterial quality of urinary tract infections in diabetic and non-diabetics of the population of Ma’an Province, Jordan. Pakistan J Biol Sci 20:179–188

    CAS  Google Scholar 

  • Alqudah AA, Tarawneh KA, Alkafaween IK, Saad SB (2014) Optimizing the biodegradation of 3, 4-dichlorobenzoic acid by Corynebacterium jeikeium. Int J Biol 6(3):54–63

    CAS  Google Scholar 

  • Althunibat OY, Qaralleh H, Al-Dalin SYA, Abboud M, Khleifat K, Majali IS, Jaafraa A (2016) Effect of thymol and carvacrol, the major components of Thymus capitatus on the growth of Pseudomonas aeruginosa. J Pure Appl Microbiol 10(1):367–374

    CAS  Google Scholar 

  • Alva VA, Peyton BM (2003) Phenol and catechol biodegradation by the haloalkaliphile Halomonas campisalis: influence of pH and salinity. Environ Sci Technol 37(19):4397–4402

    CAS  PubMed  Google Scholar 

  • Bakhshi Z, Najafpour G, Kariminezhad E, Pishgar R, Mousavi N, Taghizade T (2011) Growth kinetic models for phenol biodegradation in a batch culture of Pseudomonas putida. Environ Technol 32(16):1835–1841

    Google Scholar 

  • Bastos AER, Tornisielo VL, Nozawa SR, Trevors JT, Rossi A (2000) Phenol metabolism by two microorganisms isolated from Amazonian forest soil samples. J Ind Microbiol Biotechnol 24(6):403–409

    CAS  Google Scholar 

  • Beshay U, Abd-El-Haleem D, Moawad H, Zaki S (2002) Phenol biodegradation by free and immobilized Acinetobacter. Biotech Lett 24(15):1295–1297

    CAS  Google Scholar 

  • Bollag JM, Shuttleworth KL, Anderson DH (1988) Laccase-mediated detoxification of phenolic compounds. Appl Environ Microbiol 54(12):3086–3091

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das B, Mandal TK, Patra S (2016) Biodegradation of phenol by a novel diatom BD1IITG-kinetics and biochemical studies. Int J Environ Sci Technol 13(2):529–542

    CAS  Google Scholar 

  • Der Yang R, Humphrey AE (1975) Dynamic and steady state studies of phenol biodegradation in pure and mixed cultures. Biotechnol Bioeng 17(8):1211–1235

    CAS  PubMed  Google Scholar 

  • Döbereiner J, Marriel IE, Nery M (1976) Ecological distribution of Spirillum lipoferum Beijerinck. Can J Microbiol 22(10):1464–1473

    PubMed  Google Scholar 

  • El-Naas M, Al-Zuhair S, Makhlouf S (2010) Batch degradation of phenol in a spouted bed bioreactor system. J Ind Eng Chem 16:267–272

    CAS  Google Scholar 

  • Ereqat SI, Abdelkader AA, Nasereddin AF, Al-Jawabreh AO, Zaid TM, Letnik I, Abdeen ZA (2018) Isolation and characterization of phenol degrading bacterium strain Bacillus thuringiensis J20 from olive waste in Palestine. J Environm Sci Health Part A 53(1):39–45

    CAS  Google Scholar 

  • Gonzalez G, Herrera G, Garcıa MT, Pena M (2001) Biodegradation of phenolic industrial wastewater in a fluidized bed bioreactor with immobilized cells of Pseudomonas putida. Biores Technol 80(2):137–142

    CAS  Google Scholar 

  • González AG, Herrador MÁ (2007) A practical guide to analytical method validation, including measurement uncertainty and accuracy profiles. TrAC Trends Anal Chem 26(3):227–238

    Google Scholar 

  • Hill GA, Milne BJ, Nawrocki PA (1996) Cometabolic degradation of 4-chlorophenol by Alcaligenes eutrophus. Appl Microbiol Biotechnol 46(2):163–168

    CAS  PubMed  Google Scholar 

  • Karigar C, Mahesh A, Nagenahalli M, Yun DJ (2006) Phenol degradation by immobilized cells of Arthrobacter citreus. Biodegradation 17(1):47–55

    CAS  PubMed  Google Scholar 

  • Khleifat KM (2006) Biodegradation of phenol by Ewingella americana: Effect of carbon starvation and some growth conditions. Process Biochem 41(9):2010–2016

    CAS  Google Scholar 

  • Khleifat KM (2007) Effect of substrate adaptation, carbon starvation and cell density on the biodegradation of phenol by Actinobacillus sp. Fresenius Environ Bull 16(7):726–730

    CAS  Google Scholar 

  • Khleifat KM, Abboud MM, Al-Mustafa AH, Al-Sharafa KY (2006a) Effects of carbon source and Vitreoscilla hemoglobin (VHb) on the production of β-galactosidase in Enterobacter aerogenes. Curr Microbiol 53(4):277

    CAS  PubMed  Google Scholar 

  • Khleifat KM, Abboud MM, Al-Mustafa AH (2006b) Effect of Vitreoscilla hemoglobin gene (vgb) and metabolic inhibitors on cadmium uptake by the heterologous host Enterobacter aerogenes. Process Biochem 41(4):930–934

    CAS  Google Scholar 

  • Khleifat K, Abboud M, Al-Shamayleh W, Jiries A, Tarawneh K (2006c) Effect of chlorination treatment on gram negative bacterial composition of recycled wastewater. Pak J Biol Sci 9:1660–1668

    CAS  Google Scholar 

  • Khleifat KM, Abboud MM, Omar SS, Al-Kurishy JH (2006d) Urinary tract infection in South Jordanian population. J Med Sci 6:5–11

    CAS  Google Scholar 

  • Khleifat KM, Shawabkeh R, Al-Majali I, Tarawneh K (2007a) Biodegradation kinetics of phenol by Klebsiella oxytoca: effect of carbon and Nitrogen source. Fresenius Environ Bull 16(5):489

    CAS  Google Scholar 

  • Khleifat K, Al-Majali I, Shawabkeh R, Tarawneh K (2007b) Effect of carbon and nitrogen sources on the biodegradation of phenol by Klebsiella oxytoca and growth kinetic characteristics. Fresenius Environ Bull 16(5):1–7

    Google Scholar 

  • Khleifat KM, Tarawneh KA, Wedyan MA, Al-Tarawneh AA, Al Sharafa K (2008) Growth kinetics and toxicity of Enterobacter cloacae grown on linear alkylbenzene sulfonate as sole carbon source. Curr Microbiol 57(4):364–370

    CAS  PubMed  Google Scholar 

  • Khleifat KM, Halasah RA, Tarawneh KA, Halasah Z, Shawabkeh R, Wedyan MA (2010) Biodegradation of linear alkylbenzene sulfonate by Burkholderia sp.: Effect of some growth conditions. Int J Agr Biol 12:17–25

    CAS  Google Scholar 

  • Khleifat KM, Sharaf EF, Al-limoun MO (2015) Biodegradation of 2-chlorobenzoic acid by Enterobacter cloacae: Growth kinetics and effect of growth conditions. Bioremediat J 19(3):207–217

    CAS  Google Scholar 

  • Kumar S, Mishra VK, Kumar U, Kumar A, Varghese S (2013) Biodegradation of phenol by bacterial strains and their catalytic ability. Intl J Agric Environ Biotechnol 6:108–115

    Google Scholar 

  • Kumaran P, Paruchuri YL (1997) Kinetics of phenol biotransformation. Water Res 31(1):11–22

    CAS  Google Scholar 

  • Lallai A, Mura G, Miliddi R, Mastinu C (1988) Effect of pH on growth of mixed cultures in batch reactor. Biotechnol Bioeng 31(2):130–134

    CAS  PubMed  Google Scholar 

  • Levén L, Schnürer A (2005) Effects of temperature on biological degradation of phenols, benzoates and phthalates under methanogenic conditions. Int Biodeterior Biodegradation 55(2):153–160

    Google Scholar 

  • Liu YJ, Zhang AN, Wang XC (2009a) Biodegradation of phenol by using free and immobilized cells of Acinetobacter sp. XA05 and Sphingomonas sp. FG03. Biochem Eng J 44:187–192

    CAS  Google Scholar 

  • Liu QS, Liu Y, Show KY, Tay JH (2009b) Toxicity effect of phenolon aerobic granules. Environ Technol 30:69–74

    PubMed  Google Scholar 

  • Liu J, Wang Q, Yan J, Qin X, Li L, Xu W, Bajpai RK (2013) Isolation and characterization of a novel phenol degrading bacterial strain WUST-C1. Ind Eng Chem Res 52(1):258–265

    CAS  Google Scholar 

  • Liu Z, Xie W, Li D, Peng Y, Li Z, Liu S (2016) Biodegradation of phenol by bacteria strain Acinetobacter calcoaceticus PA isolated from phenolic wastewater. Int J Environ Res Public Health 13(3):300

    PubMed Central  Google Scholar 

  • Loh KC, Wang SJ (1997) Enhancement of biodegradation of phenol and a nongrowth substrate 4-chlorophenol by medium augmentation with conventional carbon sources. Biodegradation 8(5):329–338

    CAS  PubMed  Google Scholar 

  • Ma Y, Prasad MN, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258. https://doi.org/10.1016/j.biotechadv.2010.12.001

    Article  CAS  PubMed  Google Scholar 

  • Mirza BS, Rodrigues JLM (2012) Development of a direct isolation procedure for free-living diazotrophs under controlled hypoxic conditions. Appl Environ Microbiol 78(16):5542–5549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra VK, Kumar N (2017) Microbial degradation of phenol: a review. Jf Water Pollut Purific Res 4(1):17–22

    CAS  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc Am J 74:533–542. https://doi.org/10.2136/sssaj2008.0240

    Article  CAS  Google Scholar 

  • Nair CI, Jayachandran K, Shashidhar S (2008) Biodegradation of phenol. African. J Biotechnol 7(25):4951–4958

    CAS  Google Scholar 

  • Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170(1):265–270

    CAS  PubMed  Google Scholar 

  • Padhi SK, Gokhale S (2017) Benzene biodegradation by indigenous mixed microbial culture: kinetic modeling and process optimization. Int Biodeterior Biodegradation 119:511–519

    CAS  Google Scholar 

  • Pawlowsky U, Howell JA (1973) Mixed culture biooxidation of phenol. I. Determination of kinetic parameters. Biotechnol Bioeng 15(5):889–896

    CAS  Google Scholar 

  • Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ (2007) O-CAS, a fast and universal method for siderophore detection. J Microbiol Methods 70(1):127–131

    PubMed  Google Scholar 

  • Rai A, Gowrishetty KK, Singh S, Chakrabarty J, Bhattacharya P, Dutta S (2021) Simultaneous bioremediation of cyanide, phenol, and Ammoniacal-N from synthetic coke-oven wastewater using Bacillus sp. NITD 19. J Environ Eng 147(1):04020143

    CAS  Google Scholar 

  • Saravanan P, Pakshirajan K, Saha P (2011) Biodegradation kinetics of phenol by predominantly Pseudomonas sp. in a batch shake flask. Desalin Water Treatm 36(1–3):99–104

    CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56

    CAS  PubMed  Google Scholar 

  • Senthilvelan T, Kanagaraj J, Panda RC, Mandal AB (2014) Biodegradation of phenol by mixed microbial culture: an eco-friendly approach for the pollution reduction. Clean Technol Environ Policy 16(1):113–126

    CAS  Google Scholar 

  • Tarawneh KA, Al-Tawarah NM, Abdel-Ghani AH, Al-Majali AM, Khleifat KM (2009) Characterization of verotoxigenic Escherichia coli (VTEC) isolates from faeces of small ruminants and environmental samples in Southern Jordan. J Basic Microbiol 49(3):310–317

    CAS  PubMed  Google Scholar 

  • Ucun H, Yildiz E, Nuhoglu A (2010) Phenol biodegradation in a batch jet loop bioreactor (JLB): Kinetics study and pH variation. Biores Technol 101(9):2965–2971

    CAS  Google Scholar 

  • Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144. https://doi.org/10.1007/s00253-006-0380-z

    Article  CAS  PubMed  Google Scholar 

  • Vílchez JI, Navas A, González-López J, Arcos SC, Manzanera M (2016) Biosafety test for plant growth-promoting bacteria: Proposed environmental and human safety index (EHSI) protocol. Front Microbiol 6:1514

    PubMed  PubMed Central  Google Scholar 

  • Vilchez S, Manzanera M (2011) Biotechnological uses of desiccation- tolerant microorganisms for the rhizoremediation of soils subjected to seasonal drought. Appl Microbiol Biotechnol 91:1297–1304. https://doi.org/10.1007/s00253-011-3461-6

    Article  CAS  PubMed  Google Scholar 

  • Wang SJ, Loh KC (1999) Modeling the role of metabolic intermediates in kinetics of phenol biodegradation. Enzyme Microb Technol 25(3–5):177–184

    Google Scholar 

  • Wang Y, Tian Y, Han B, Zhaw HB, Bi JN, Cai BL (2007) Biodegradation of phenol by free and immobilized Acinetobacter sp. strain PD12. J Environ Sci 19:222–225

    CAS  Google Scholar 

  • Wen Y, Li C, Song X, Yang Y (2020) Biodegradation of Phenol by Rhodococcus sp. Strain SKC: Characterization and Kinetics Study. Molecules 25(16):3665

    CAS  PubMed Central  Google Scholar 

  • Younis SA, El-Gendy NS, Nassar HN (2020) Biokinetic aspects for biocatalytic remediation of xenobiotics polluted seawater. J Appl Microbiol 129(2):319–334

    CAS  PubMed  Google Scholar 

  • Zeng HY, Cao XL, Xiong LB, Cai XL, Huang LQ, Zhang CY, Li YQ (2014) Microbiological degradation of phenol using two co-aggregating bacterial strains. Environ Earth Sci 71(3):1339–1348

    CAS  Google Scholar 

  • Zhao G, Zhou L, Li Y, Liu X, Ren X, Liu X (2009) Enhancement of phenol degradation using immobilized microorganisms and organic modified montmorillonite in a two-phase partitioning bioreactor. J Hazard Mater 169:402–410

    CAS  PubMed  Google Scholar 

  • Zumriye A, Gultac B (1999) Determination of the effective diffusion coefficient of phenol in calcium alginate immobilized Pseudomonas putida. Enzyme Microb Technol 25:344–348

    Google Scholar 

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Acknowledgements

We gratefully acknowledge Mutah university for their support and their help.

Funding

Authors would like to thank Deanship of Scientific Research, Mutah University, Jordan for supporting this work with grant proposal number 2020/316.

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Authors and Affiliations

  1. Prince Faisal Center for Dead Sea, Environmental and Energy Research, Mutah University, Al-Karak, Jordan

    Amjad Al-Tarawneh

  2. Department of Biology, College of Science, Mutah University, Al-Karak, 61710, Jordan

    Khaled M. Khleifat & Kholoud Shiyyab

  3. Faculty of Allied Medical Sciences, Al-Ahliyya Amman University, Amman, 19328, Jordan

    Khaled M. Khleifat

  4. Department of Chemistry, Al-Balqa Applied University, Al-Salt, 19117, Jordan

    Ibrahim N. Tarawneh

  5. Department of Chemistry, College of Science, Mutah University, Al-Karak, Jordan

    Tayel El-Hasan

  6. Territorial and Production Systems Sustainability Department, ENEA, via Anguillarese 301, 00123, Rome, Italy

    Anna Rosa Sprocati, Chiara Alisi & Flavia Tasso

  7. Pharmacological and Diagnostic Research Center (PDRC), Faculty of Pharmacy, Al-Ahliyya Amman University, Amman, 19328, Jordan

    Moath Alqaraleh

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  1. Amjad Al-Tarawneh
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Al-Tarawneh, A., Khleifat, K.M., Tarawneh, I.N. et al. Phenol biodegradation by plant growth promoting bacterium, S. odorifera: kinetic modeling and process optimization. Arch Microbiol 204, 104 (2022). https://doi.org/10.1007/s00203-021-02691-y

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