Plant Growth-Promoting Rhizobium Nepotum Phenol Utilization: Characterization and Kinetics

Haitham Qaralleh, Khaled M. Khleifat, Maha N. Abu Hajleh, Muhamad O. Al-Limoun, Rawan Alshawawreh, Mousa K. Magharbeh, Talal Salem Al-Qaisi, Husni S. Farah, Tayel ElHasan, Amjad Al-Tarawneh, Salah H. Aljbour, Moath Alqaraleh

Abstract

Phenol is a severe pollutant that harms the environment and, potentially, human health. This study aimed to investigate the biodegradability of phenol by the plant growth-promoting bacterium R. nepotum. That included studying the growth kinetics and the effects of growth conditions such as incubation temperature, pH, and the use of different substrate concentrations. As the primary substrate, six different starting concentrations of phenol were utilized. The ability of these cells to biodegrade phenol was greatly influenced by the culture conditions. After 36 and 96 hours of incubation at pH 7 and a temperature of 28 C, this organism grew the fastest and had the highest phenol biodegradation. The biodegradation rate is much higher at 700 mg/L, the highest of the six concentrations tried. In less than 96 hours of incubation, more than 90% of the phenol (700 mg/L) had been eliminated. The Haldane model has been the most accurate for determining the relationship between the initial concentration of phenol and growth rate. In contrast, the refined Gompertz model provided the most accurate depiction of phenol biodegradation over time. As predicted by the Haldane equation, the highest specific growth rate, half-saturation coefficient, and Haldane's growth kinetics inhibition coefficient are 0.7161 h1, 15.8 parts per million (ppm), and 292 parts per million (ppm), respectively. The equation of Haldane successfully fitted the experimental data by reducing the SSR (sum of squared errors) to 3.8x10 3. According to the results of the analysis by GC-MS for the bacterial culture sample, the hydroxylase enzyme was the first to convert the phenol molecule into catechol. The catechol was subsequently broken down into 2-hydroxymucconic semialdehyde by the 2,3-dioxygenase enzyme, which occurred through the meta-pathway. It is the first study showing that R. nepotum, a plant growth promoter, has high efficiency of phenol. In phenol-stressed conditions, this could help with rhizoremediation and crop yield preservation.


Keywords: Rhizobium nepotum, phenol, biodegradation, kinetics, plant growth-promoting bacteria.

 

https://doi.org/10.55463/issn.1674-2974.49.4.11

 


Full Text:

PDF


References


BESHAY U., ABD-EL-HALEEM D., MOAWAD H., and ZAKI S. Phenol biodegradation by free and immobilized Acinetobacter. Biotechnology Letters, 2002, 24: 1295–1297. https://doi.org/10.1023/A:1016222328138

KHLEIFAT K., & ABBOUD M. M. Correlation between bacterial haemoglobin gene (vgb) and aeration: their effect on the growth and α‐amylase activity in transformed Enterobacter aerogenes. Journal of Applied Microbiology, 2003, 94: 1052–1058. https://doi.org/10.1046/j.1365-2672.2003.01939.x

KHLEIFAT K. M. Biodegradation of phenol by Actinobacillus sp.: Mathematical interpretation and effect of some growth conditions. Bioremediation Journal, 2007, 11: 103–112. https://doi.org/10.1080/10889860701429328

KHLEIFAT K. M. Effect of substrate adaptation, carbon starvation and cell density on the biodegradation of phenol by Actinobacillus sp. Fresenius Environmental Bulletin, 2007, 16: 726–730. https://www.researchgate.net/publication/286110289_Effect_of_substrate_adaptation_carbon_starvation_and_cell_density_on_the_biodegradation_of_phenol_by_Actinobacillus_sp

AISAMI A., YASID N. A., and ABD SHUKOR M. Y. Optimization of cultural and physical parameters for phenol biodegradation by newly identified Pseudomonas Sp. AQ5-04. Journal of Tropical Life Science, 2020, 10: 223–233. https://doi.org/10.11594/jtls.10.03.06

KHLEIFAT K. M., TARAWNEH K. A., ALI WEDYAN M., AL-TARAWNEH A. A., and AL SHARAFA K. Growth kinetics and toxicity of Enterobacter cloacae grown on linear alkylbenzene sulfonate as sole carbon source. Current Microbiology, 2008, 57: 364–470. https://doi.org/10.1007/s00284-008-9203-z

EL-NAAS M. H., AL-ZUHAIR S., and MAKHLOUF S. Batch degradation of phenol in a spouted bed bioreactor system. Journal of Industrial and Engineering Chemistry, 2010, 16: 267–272. https://doi.org/10.1016/j.jiec.2009.09.072

ABBOUD M. M., ALJUNDI I. H., KHLEIFAT K. M., and DMOUR S. Biodegradation kinetics and modeling of whey lactose by bacterial hemoglobin VHb-expressing Escherichia coli strain. Biochemical Engineering Journal, 2010, 48: 166–172. https://doi.org/10.1016/j.bej.2009.09.006

KHLEIFAT K., HOMADY M. H., TARAWNEH K. A., and SHAKHANBEH J. Effect of Ferula hormonis extract on social aggression, fertility and some physiological parameters in prepubertal male mice. Endocrine Journal, 2001, 48: 473–482. https://doi.org/10.1507/endocrj.48.473

KHLEIFAT K. M., ABBOUD M. M., AL-MUSTAFA A. H., and AL-SHARAFA K. Y. Effects of carbon source and Vitreoscilla hemoglobin (VHb) on the production of β-galactosidase in Enterobacter aerogenes. Current Microbiology, 2006, 53: 277–281. https://doi.org/10.1007/s00284-005-0466-3

KHLEIFAT K. M., ABBOUD M. M., and AL-MUSTAFA A. H. Effect of Vitreoscilla hemoglobin gene (vgb) and metabolic inhibitors on cadmium uptake by the heterologous host Enterobacter aerogenes. Process Biochemistry, 2006, 41: 930–934. https://doi.org/10.1016/j.procbio.2005.10.012

KHLEIFAT K. M., ABBOUD M. M., OMAR S. S., and AL-KURISHY J. H. Urinary tract infection in South Jordanian population. Journal of Medical Sciences, 2006, 6: 5–11. https://doi.org/10.3923/jms.2006.5.11

TARAWNEH K. A., AL‐TAWARAH N., ABDEL‐GHANI A. H., AL‐MAJALI A. M., and KHLEIFAT K. M. Characterization of verotoxigenic Escherichia coli (VTEC) isolates from faeces of small ruminants and environmental samples in Southern Jordan. Journal of Basic Microbiology, 2009, 49: 310–317. https://doi.org/10.1002/jobm.200800060

TARAWNEH K. A., IRSHAID F., JARAN A. S., EZEALARAB M., and KHLEIFAT K. M. Evaluation of antibacterial and antioxidant activities of methanolic extracts of some medicinal plants in northern part of Jordan. Journal of Biological Sciences, 2010, 10: 325–332. https://doi.org/10.3923/jbs.2010.325.332

ALTHUNIBAT O. Y., QARALLEH Q., AL-DALIN S. Y. A., ABBOUD M., KHLEIFAT K., MAJALI I. S., SUSANTI D., DALAEEN H., DALAEEN S., AL-DALIN A., and RAYYAN W. A. Effect of Thymol and Carvacrol, the Major Components of Thymus capitatus on the Growth of Pseudomonas aeruginosa. Journal of Pure and Applied Microbiology, 2016, 10: 367–374. https://www.microbiologyjournal.org/download/25300/

AL-ASOUFI A., KHLAIFAT A., AL TARAWNEH A., ALSHARAFA K., AL-LIMOUN M., and KHLEIFAT K. Bacterial Quality of Urinary Tract Infections in Diabetic and Non Diabetics of the Population of Ma’an Province, Jordan. Pakistan Journal of Biological Sciences, 2017, 20: 179–188. https://doi.org/10.3923/pjbs.2017.179.188

KHLEIFAT K. M., SHARAF E. F., and AL-LIMOUN M. O. Biodegradation of 2-chlorobenzoic acid by enterobacter cloacae: Growth kinetics and effect of growth conditions. Bioremediation Journal, 2015, 19: 207–217. https://doi.org/10.1080/10889868.2015.1029113

VÍLCHEZ J. I., NAVAS A., GONZÁLEZ-LÓPEZ J., ARCOS S. C., and MANZANERA M. Biosafety test for plant growth-promoting bacteria: Proposed environmental and human safety index (EHSI) protocol. Frontiers in Microbiology, 2016, 6: 1514. https://doi.org/https://doi.org/10.3389/fmicb.2015.01514

VILCHEZ S., & MANZANERA M. Biotechnological uses of desiccation-tolerant microorganisms for the

rhizoremediation of soils subjected to seasonal drought. Applied Microbiology and Biotechnology, 2011, 91: 1297–1304. https://doi.org/10.1007/s00253-011-3461-6

IMRAN A., SAADALLA M. J. A., KHAN S.-U., MIRZA M. S., MALIK K. A., and HAFEEZ F. Y. Ochrobactrum sp. Pv2Z2 exhibits multiple traits of plant growth promotion, biodegradation and N-acyl-homoserine-lactone quorum sensing. Annals of Microbiology, 2014, 64: 1797–1806. https://doi.org/https://doi.org/10.1007/s13213-014-0824-0

PUŁAWSKA J., WILLEMS A., DE MEYER S. E., and SÜLE S. Rhizobium nepotum sp. nov. isolated from tumors on different plant species. Systematic and Applied Microbiology, 2012, 35: 215–220. https://doi.org/10.1016/j.syapm.2012.03.001

PATTEN C. L., and GLICK B. R. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Applied and Environmental Microbiology, 2002, 68: 3795–3801. https://doi.org/10.1128/AEM.68.8.3795-3801.2002

NITHYAPRIYA S., LALITHA S., SAYYED R. Z., REDDY M. S., DAILIN D. J., El ENSHASY H. A., SURIANI N. L., and HERLAMBANG S. Production, purification, and characterization of bacillibactin siderophore of Bacillus subtilis and its application for improvement in plant growth and oil content in sesame. Sustainability, 2021, 13: 5394. https://doi.org/10.3390/su13105394

CUEVA-YESQUÉN L. G., GOULART M. C., DE ANGELIS A. D., NOPPER ALVES M., and FANTINATTI-GARBOGGINI F. Multiple plant growth-promotion traits in endophytic bacteria retrieved in the vegetative stage from passionflower. Frontiers in Plant Science, 2021, 11: 621740. https://doi.org/10.3389/fpls.2020.621740

DAS B., MANDAL T. K., and PATRA S. Biodegradation of phenol by a novel diatom BD1IITG-kinetics and biochemical studies. International Journal of Environmental Science and Technology, 2016, 13: 529–542. https://doi.org/10.1007/s13762-015-0857-3

LOH K.-C., & WANG S.-J. Enhancement of biodegradation of phenol and a nongrowth substrate 4-chlorophenol by medium augmentation with conventional carbon sources. Biodegradation, 1997, 8: 329–338. https://doi.org/10.1023/a:1008267607634

KHLEIFAT K. M., HALASAH R. A., TARAWNEH K. A., HALASAH Z., SHAWABKEH R., and WEDYAN M. A. Biodegradation of linear alkylbenzene sulfonate by Burkholderia sp.: Effect of some growth conditions. International Journal of Agriculture and Biology, 2010, 12: 17–25. https://www.researchgate.net/publication/258975141_Biodegradation_of_Linear_Alkylbenzene_Sulfonate_by_Burkholderia_sp_Effect_of_Some_Growth_Conditions

SHAWABKEH R., KHLEIFAT K. M., AL-MAJALI I., and TARAWNEH K. Rate of biodegradation of phenol by Klebsiella oxytoca in minimal medium and nutrient broth conditions. Bioremediation Journal, 2007, 11: 13–19. https://doi.org/10.1080/10889860601185830

YOUSSEF M., EL-SHATOURY E. H., ALI S. S., and EL-TAWEEL G. E. Enhancement of phenol degradation by free and immobilized mixed culture of Providencia stuartii PL4 and Pseudomonas aeruginosa PDM isolated from activated sludge. Bioremediation Journal, 2019, 23: 53–71. https://doi.org/10.1080/10889868.2019.1602106

GONZALEZ G., HERRERA G., GARCIA M. T., and PENA M. Biodegradation of phenolic industrial wastewater in a fluidized bed bioreactor with immobilized cells of Pseudomonas putida. Bioresource Technology, 2001, 80: 137–142. https://doi.org/10.1016/s0960-8524(01)00076-1

MIRZA B. S., & RODRIGUES J. L. M. Development of a direct isolation procedure for free-living diazotrophs under controlled hypoxic conditions. Applied and Environmental Microbiology, 2012, 78(16): 5542–5549. https://doi.org/10.1128/AEM.00714-12

SARAVANAN T., MUTHUSAMY M., and MARIMUTHU T. Effect of Pseudomonas fluorescens on Fusarium wilt pathogen inbanana rhizosphere. Journal of Biological Sciences, 2004, 4: 192–198. https://dx.doi.org/10.3923/jbs.2004.192.198 [33] PAWLOWSKY U., & HOWELL J. A. Mixed culture biooxidation of phenol. I. Determination of kinetics parameters. Biotechnology and Bioengineering, 1973, 15: 889–896. https://doi.org/10.1002/bit.260150506 [34] KUMARAN P., & PARUCHURI Y. L. Kinetics of phenol biotransformation. Water Research, 1997, 31: 11-22. https://doi.org/10.1016/S0043-1354(99)80001-3

WEN Y., LI C., SONG X., and YANG Y. Biodegradation of phenol by Rhodococcus sp. strain SKC: Characterization and kinetics study. Molecules, 2020, 25: 3665. https://doi.org/10.3390/molecules25163665

[ 35 ] LIU J., WANG Q., YAN J., QIN X., LI L., XU W., SUBRAMANIAM R., and BAJPAI R. K. Isolation and characterization of a novel phenol degrading bacterial strain WUST-C1. Industrial and Engineering Chemistry Research, 2013, 52: 258-265. https://doi.org/10.1021/ie3012903

EREQAT S. I., ABDELKADER A. A., NASEREDDIN A. F., AL-JAWABREH A. O., ZAID T. M., LETNIK I., and ABDEEN Z. Isolation and characterization of phenol degrading bacterium strain Bacillus thuringiensis J20 from olive waste in Palestine. Journal of Environmental Science and Health Part A, 2018, 53: 39–45. https://doi.org/10.1080/10934529.2017.1368300

LEVEN L., & SCHNÜRER A. Effects of temperature on biological degradation of phenols, benzoates and phthalates under methanogenic conditions. International Biodeterioration & Biodegradation, 2005, 55: 153–160. https://doi.org/10.1016/j.ibiod.2004.09.004

ALJUNDI I. H., & KHLEIFAT K. M. Biosorption of lead by E. coli strains expressingVitreoscilla hemoglobin: Isotherm modeling with two‐and three‐parameter models. Engineering in Life Sciences, 2010, 10: 225–232. https://doi.org/10.1002/elsc.200900092

ONYSKO K. A., BUDMAN H. M., and ROBINSON C. W. Effect of temperature on the inhibition kinetics of phenol biodegradation by Pseudomonas putida Q5. Biotechnology and Bioengineering, 2000, 70: 291–299. https://doi.org/10.1002/1097-0290(20001105)70:3<291::aid-bit6>3.0.co;2-y

KHLEIFAT K., ABBOUD M., AL-SHAMAYLEH W., JIRIES A., and TARAWNEH K. Effect of chlorination treatment on gram negative bacterial composition of recycled wastewater. Pakistan Journal of Biological Sciences, 2006, 9: 1660–1668. https://doi.org/10.3923/pjbs.2006.1660.1668

MARKS T. S., SMITH A. R. W., and QUIRK A. V. Degradation of 4-chlorobenzoic acid by Arthrobacter sp. Applied and Environmental Microbiology, 1984, 48: 1020–1025. https://doi.org/10.1128/aem.48.5.1020-1025.1984

ALVA V. A., & PEYTON B. M. Phenol and catechol biodegradation by the haloalkaliphile Halomonas campisalis: influence of pH and salinity. Environmental Science & Technology, 2003, 37: 4397–4402. https://doi.org/10.1021/es0341844

SUHAILA Y. N., HASDIANTY A., MAEGALA N. M., AQLIMA A., HAZWAN A. H., ROSFARIZAN M., and ARIFF A. B. Biotransformation using resting cells of Rhodococcus UKMP-5M for phenol degradation. Biocatalysis and Agricultural Biotechnology, 2019, 21: 101309. https://doi.org/10.1016/j.bcab.2019.101309

KE Z., XIANGLING W., JIAN C., and JIA C. Biodegradation of diethyl phthalate by Pseudomonas sp. BZD-33 isolated from active sludge. IOP Conference Series: Earth and Environmental Science, 2019, 295: 12070. https://doi.org/10.1088/1755-1315/295/2/012070

ZOU S., ZHANG B., YAN N., ZHANG C., XU H., ZHANG Y., and RITTMAN B. E. Competition for molecular oxygen and electron donor between phenol and quinoline during their simultaneous biodegradation. Process Biochemistry, 2018, 70: 136–143. https://doi.org/10.1016/j.procbio.2018.04.015

ABBOUD M. M., KHLEIFAT K. M., BATARSEH M., TARAWNEH K. A., AL-MUSTAFA A., and AL-MADADHAH M. 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 and Microbial Technology, 2007, 41: 432–439. https://doi.org/10.1016/j.enzmictec.2007.03.011

SAMADI A., SHARIFI H., GHOBADI NEJAD Z., HASAN-ZADEH A., and YAGHMAEI S. Biodegradation of 4-Chlorobenzoic acid by Lysinibacillus macrolides DSM54T and determination of optimal conditions. International Journal of Environmental Research, 2020, 14: 145–154. https://doi.org/10.1007/s41742-020-00247-4


Refbacks

  • There are currently no refbacks.