Characterization and Potential of Plant Growth-Promoting Rhizobacteria (PGPR) Isolates Capacity Correlating with Their Hydrocarbon Biodegradation Capability

Pujawati Suryatmana, Mieke Rochimi Setiawati, Diyan Herdiyantoro, Betty Natalie Fitriatin, Nadia Nuraniya Kamaluddin


The aim of this research is to find the characteristics of three PGPR isolates—Azospirillum sp., Bacillus sp., and Pseudomonas sp.: First, by profiling their characteristics in a liquid bioremediation system and secondly by measuring their performance as a bioagent in a soil phytoremediation system using ramie plant (Boehmia niviea L.). A Randomized Block Design in triplicate is used: (1) a Nitrogenfree medium with mineral media containing 1% (wt/v) petroleum hydrocarbons; and (2) 1% (wt/v) glucose medium as control. We tested their petroleum-degrading capacity, nitrogenase activity, phytohormones production, and ramie plant growth. The results showed that both Pseudomonas sp. (98.7%, 81.78% degradation efficiency) and Azospirillum sp. (93.80%, 83.70%) were the superior candidate in both systems. They both show reduced but adequate phytohormone production, managing to improve ramie plant growth. Both also showed reduced but sufficient nitrogen fixing capabilities to improve hydrocarbon degradation activity effectively. Meanwhile, Bacillus sp. has the lowest biodegradation capabilities (84.07%; 78.6%) and lowest nitrogenase activity, while failing to improve plant growth. Therefore Bacillus sp. would be more beneficial in a bacterial consortium where its characteristics (high IAA production) can be coupled with other isolates that can offset its lack of phytohormone or nitrogenase activity.


Azospirillum sp.; Bacillus sp.; Hydrocarbon-degradation; PGPR; Pseudomonas sp.

Full Text:



Abbasian, F., Lockington, R., Mallavarapu, M., & Naidu, R. (2015). A comprehensive review of aliphatic hydrocarbon biodegradation by bacteria. Applied Biochemistry and Biotechnology, 176, 670–699. DOI

Al-Dhabaan, F. A. (2019). Morphological, biochemical and molecular identification of petroleum hydrocarbons biodegradation bacteria isolated from oil polluted soil in Dhahran, Saud Arabia. Saudi Journal of Biological Sciences, 26(6), 1247–1252. DOI

Al-Mailem, D. M., Kansour, M. K., & Radwan, S. S. (2019). Cross-bioaugmentation among four remote soil samples contaminated with oil exerted just inconsistent effects on oil-bioremediation. Frontiers in Microbiology, 10, 1–11. DOI

Alotaibi, F., St-Arnaud, M., & Hijri, M. (2022). In-depth characterization of plant growth promotion potentials of selected alkanes-degrading plant growth-promoting bacterial isolates. Frontiers in Microbiology, 2022, 863702. DOI

Babalola, O. O., & Akindolire, A. M. (2011). Identification of native rhizobacteria peculiar to selected food crops in Mmabatho municipality of South Africa. Biological Agriculture and Horticulture, 27(3–4), 294–309. DOI

Backer, R., Rokem, J. S., Ilangumaran, G., Lamont, J., Praslickova, D., Ricci, E., … Smith, D. L. (2018). Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Frontiers in Plant Science, 871, 1–17. DOI

Bahat-Samet, E., Castro-Sowinski, S., & Okon, Y. (2004). Arabinose content of extracellular polysaccharide plays a role in cell aggregation of Azospirillum brasilense. FEMS Microbiology Letters, 237(2), 195–203. DOI

Bakaeva, M., Kuzina, E., Vysotskaya, L., Kudoyarova, G., Arkhipova, T., Rafikova, G., … Loginov, O. (2020). Capacity of Pseudomonas strains to degrade hydrocarbons, produce auxins and maintain plant growth under normal conditions and in the presence of petroleum contaminants. Plants, 9(3), 379. DOI

Baldera-Moreno, Y., Pino, V., Farres, A., Banerjee, A., Gordillo, F., & Andler, R. (2022). Biotechnological aspects and mathematical modeling of the biodegradation of plastics under controlled conditions. Polymers, 14(3), 375. DOI

Bano, A., Shahzad, A., & Siddiqui, S. (2015). Rhizodegradation of hydrocarbon from oily sludge. Journal of Bioremediation & Biodegradation, 6, 289. DOI

Bashan, Y., Puente, M. E., de-Bashan, L. E., & Hernandez, J.-P. (2008). Environmental uses of plant growth-promoting bacteria. In E. A. Barka, & C. Clément (Eds.), Plant-Microbe Interactions (pp. 69–93). Retrieved from PDF

Beškoski, V. P., Gojgić-Cvijović, G., Milić, J., Ilić, M., Miletić, S., Šolević, T., & Vrvić, M. M. (2011). Ex situ bioremediation of a soil contaminated by mazut (heavy residual fuel oil) - A field experiment. Chemosphere, 83(1), 34–40. DOI

Bhatt, P. V., & Vyas, B. R. M. (2014). Screening and characterization of plant growth and health promoting rhizobacteria. International Journal of Current Microbiology and Applied Sciences, 3(6), 139–155. Retrieved from PDF

Bible, A. N., Khalsa-Moyers, G. K., Mukherjee, T., Green, C. S., Mishra, P., Purcell, A., … Alexandre, G. (2015). Metabolic adaptations of Azospirillum brasilense to oxygen stress by cell-to-cell clumping and flocculation. Applied and Environmental Microbiology, 81(24), 8346–8357. DOI

BPS. (2020). Statistik pertambangan non minyak dan gas bumi 2014 – 2019. Jakarta, ID: Badan Pusat Statistik. Retrieved from website

Burdman, S., Okon, Y., & Jurkevitch, E. (2000). Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Critical Reviews in Microbiology, 26(2), 91–110. DOI

Cruz-Hernández, M. A., Mendoza-Herrera, A., Bocanegra-García, V., & Rivera, G. (2022). Azospirillum spp. from plant growth-promoting bacteria to their use in bioremediation. Microorganisms, 10(5), 1057. DOI

Das, N., & Chandran, P. (2011). Microbial degradation of petroleum hydrocarbon contaminants: An overview. Biotechnology Research International, 2011, 941810. DOI

de-Bashan, L. E., Hernandez, J.-P., & Bashan, Y. (2012). The potential contribution of plant growth-promoting bacteria to reduce environmental degradation - A comprehensive evaluation. Applied Soil Ecology, 61, 171–189. DOI

Egamberdieva, D., Wirth, S. J., Alqarawi, A. A., Abd-Allah, E. F., & Hashem, A. (2017). Phytohormones and beneficial microbes: Essential components for plants to balance stress and fitness. Frontiers in Microbiology, 8, 1–14. DOI

Essien, J., Udoukpo, F., Etesin, U., & Etuk, H. (2013). Activities of hydrocarbon-utilizing and diazotrophic bacteria in crude oil impacted mangrove sediments of the Qua Iboe Estuary, Nigeria. Geosystem Engineering, 16(2), 165–174. DOI

Gkorezis, P., Daghio, M., Franzetti, A., Van Hamme, J. D., Sillen, W., & Vangronsveld, J. (2016). The interaction between plants and bacteria in the remediation of petroleum hydrocarbons: An environmental perspective. Frontiers in Microbiology, 7, 1–27. DOI

Glick, B. R. (2003). Phytoremediation: Synergistic use of plants and bacteria to clean up the environment. Biotechnology Advances, 21(5), 383–393. DOI

Glick, B. R. (2012). Plant growth-promoting bacteria: Mechanisms and applications. Scientifica, 2012, 1-15. DOI

Gohil, R. B., Raval, V. H., Panchal, R. R., & Rajput, K. N. (2022). Plant growth-promoting activity of Bacillus sp. PG-8 isolated from fermented panchagavya and its effect on the growth of Arachis hypogea. Frontiers in Agronomy, 2022, 805454. DOI

Hansda, A., Kumar, V., Anshumali, & Usmani, Z. (2014). Phytoremediation of heavy metals contaminated soil using plant growth promoting rhizobacteria (PGPR): A current perspective. Recent Research in Science and Technology, 6(1), 131–134. Retrieved from website

Herridge, D. F., & Peoples, M. B. (1990). Ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by 15N methods. Plant Physiology, 93(2), 495-503. DOI

Hontzeas, N., Zoidakis, J., Glick, B. R., & Abu-Omar, M. M. (2004). Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium Pseudomonas putida UW4: A key enzyme in bacterial plant growth promotion. Biochimica et Biophysica Acta - Proteins and Proteomics, 1703(1), 11–19. DOI

Huang, X.-D., El-Alawi, Y., Penrose, D. M., Glick, B. R., & Greenberg, B. M. (2004). A multi-process phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environmental Pollution, 130(3), 465–476. DOI

Iqbal, A., Arshad, M., Karthikeyan, R., Gentry, T. J., Rashid, J., Ahmed, I., & Schwab, A. P. (2019). Diesel degrading bacterial endophytes with plant growth promoting potential isolated from a petroleum storage facility. 3 Biotech, 9(1), 1–12. DOI

Keputusan Menteri. (2003). Nomor 128 Tahun 2003 Tentang tata cara dan persyaratan teknis pengolahan limbah minyak bumi dan tanah terkontaminasi oleh minyak bumi secara biologis. Retrieved from PDF

Khan, S., Afzal, M., Iqbal, S., & Khan, Q. M. (2013). Plant-bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere, 90(4), 1317–1332. DOI

Kundan, R., Pant, G., Jadon, N., & Agrawal, P. K. (2015). Plant growth promoting rhizobacteria: Mechanism and current prospective. Journal of Fertilizers & Pesticides, 6, 155. DOI

Lerner, A., Castro-Sowinski, S., Valverde, A., Lerner, H., Dror, R., Okon, Y., & Burdman, S. (2009). The Azospirillum brasilense Sp7 noeJ and noeL genes are involved in extracellular polysaccharide biosynthesis. Microbiology, 155(12), 4058–4068. DOI

Liu, W., Sun, J., Ding, L., Luo, Y., Chen, M., & Tang, C. (2013). Rhizobacteria (Pseudomonas sp. SB) assist phytoremediation of oily-sludge-contaminated soil by tall fescue (Testuca arundinacea L.). Plant and Soil, 371(1–2), 533–542. DOI

Muratova, A. Y., Turkovskaya, O. V., Antonyuk, L. P., Makarov, O. E., Pozdnyakova, L. I., & Ignatov, V. V. (2005). Oil-oxidizing potential of associative rhizobacteria of the genus Azospirillum. Microbiology, 74, 210–215. DOI

Patel, T., & Saraf, M. (2017). Biosynthesis of phytohormones from novel rhizobacterial isolates and their in vitro plant growth-promoting efficacy. Journal of Plant Interactions, 12(1), 480-487. DOI

Ponmurugan, P., & Gopi, C. (2006). In vitro production of growth regulators and phosphatase activity by phosphate solubilizing bacteria. African Journal of Biotechnology, 5(4), 348–350. Retrieved from website

Saeki, H., Sasaki, M., Komatsu, K., Miura, A., & Matsuda, H. (2009). Oil spill remediation by using the remediation agent JE1058BS that contains a biosurfactant produced by Gordonia sp. strain JE-1058. Bioresource Technology, 100(2), 572-577. DOI

Salleh, A. B., Ghazali, F. M., Abd Rahman, R. N. Z., & Basri, M. (2003). Bioremediation of petroleum hydrocarbon pollution. Indian Journal of Biotechnology, 2, 411-425. Retrieved from website

Sayyed, R. Z., & Patel, P. R. (2011). Soil microorganisms and environmental health. International Journal of Biosciences and Biotechnology, 1(1), 41–66. Retrieved from website

Sinha, S., & Mukherjee, S. K. (2008). Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Current Microbiology, 56(1), 55–60. DOI

Vanbleu, E., Choudhury, B. P., Carlson, R. W., & Vanderleyden, J. (2005). The nodPQ genes in Azospirillum brasilense Sp7 are involved in sulfation of lipopolysaccharides. Environmental Microbiology, 7(11), 1769–1774. DOI

Varjani, S. J., & Upasani, V. N. (2016). Carbon spectrum utilization by an indigenous strain of Pseudomonas aeruginosa NCIM 5514: Production, characterization and surface active properties of biosurfactant. Bioresource Technology, 221, 510-516. DOI

Viñas, M., Sabaté, J., Espuny, M. J., & Solanas, A. M. (2005). Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Applied and Environmental Microbiology, 71(11), 7008–7018. DOI

Whyte, L. G., Hawari, J., Zhou, E., Bourbonnière, L., Inniss, W. E., & Greer, C. W. (1998). Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Applied and Environmental Microbiology, 64(7), 2578-2584. DOI

Wilkes, H., Buckel, W., Golding, B. T., & Rabus, R. (2016). Metabolism of hydrocarbons in n-alkane-utilizing anaerobic bacteria. Journal of Molecular Microbiology and Biotechnology, 26(1-3), 138-151. DOI

Yateem, A., Al-Sharrah, T., & Bin-Haji, A. (2007). Investigation of microbes in the rhizosphere of selected grasses for rhizoremediation of hydrocarbon-contaminated soils. Soil and Sediment Contamination, 16(3), 269–280. DOI

Zaidi, A., Khan, M., Ahemad, M., & Oves, M. (2009). Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiologica et Immunologica Hungarica, 56(3), 263–284. DOI

Zhang, X., Xu, D., Yang, G., Zhang, H., Li, J., & Shim, H. (2012). Isolation and characterization of rhamnolipid producing Pseudomonas aeruginosa strains from waste edible oils. African Journal of Microbiology Research, 6(7), 1466–1471. DOI

Zhao, D., Liu, C., Liu, L., Zhang, Y., Liu, Q., & Wu, W.-M. (2011). Selection of functional consortium for crude oil-contaminated soil remediation. International Biodeterioration and Biodegradation, 65(8), 1244–1248. DOI

Zhuang, X., Chen, J., Shim, H., & Bai, Z. (2007). New advances in plant growth-promoting rhizobacteria for bioremediation. Environment International, 33(3), 406–413. DOI


Copyright (c) 2022 The Author(s)

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.