Heavy metal, salinity and azo dye tolerant, Cr (VI) reducing, plant growth-promoting Pseudomonas aeruginosa R32 reverses Cr (VI) biotoxic effects in Vigna mungo
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Abstract
Hexavalent chromium [Cr (VI)], derived from various industries, including fly ash from coal-based Thermal Power Plants, can be a source of toxic pollution of land and water bodies. This study aimed to bioremediation of such pollutant dump sites using bacteria capable of both Cr(VI) reduction and plant growth-enhancing substance production. The bacteria were isolated from the rhizospheric fly ash of a Thermal Power Plant, Kanpur. One of the rhizospheric isolate, Pseudomonas aeruginosa R32 showed high minimum inhibitory concentration (MIC) for Cr(VI) (1250 µg/ml), heavy metal tolerance (ZnCl2, CdCl2, Pb(NO3)2) up to 100 µg/ml, Acid Red 249 (AR) tolerance and halotolerance (6% NaCl). The isolate R32 also produces plant growth-promoting (PGP) hormones in the absence or presence of Cr (VI). R32 could completely reduce Cr(VI) at a tested dose of 100 and 500 μg/ml after 24h and 72h, respectively. However, decolorization of AR was observed after 48 hours at an initial concentration of 100 µg/ml and confirmed by Fourier transform infrared spectroscopy analysis. Vigna mungo seed inoculation with isolate R32 showed increased rootling growth compared to shoot after 7 d treatment with 0, 100, 500, and 1000 μg/ml of Cr(VI) concentrations, respectively. Root length tolerance index in Cr(VI) treated V. mungo seedlings was reduced to 56%, 35%, and 29%, respectively, when treated with 100, 500, and 1000 μg/ml Cr(VI) in comparison to control. Cr(VI) sub-MIC concentrations can affect the plant growth-promoting properties of rhizospheric bacteria. Herein, we report the isolation of rhizospheric bacteria P. aeruginosa R32 showing concurrent PGP substance production and Cr(VI) bioreduction capabilities in the presence of PGP inhibitory Cr(VI) concentrations.
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Keywords
Cr(VI) bioreduction, Heavy metal toxicity, Plant growth promotion, Pseudomonas aeruginosa, Vigna mungo
References
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Bodor, A., Bounedjoum, N., Vincze, G.E., Erdeiné, Kis. Á., Laczi, K., Bende, G., et al. (2020). Challenges of unculturable bacteria: environmental perspectives. Rev Environ Sci Biotechnol, 19:1–22. https://doi.org/10.1007/s11157-020-09522-4
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Garg, S.K., Tripathi, M. & Srinath, T. (2012). Strategies for chromium bioremediation of tannery effluent. Rev Environ Contam Toxicol, 217:75–140. https://doi.org/10.1007/978-1-4614-2329-4_2
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Kumar, V., Omar, R.A., Umrao, P.D. & Kaistha, S.D. (2020). Cr(VI) toxicity inhibits microbe enhanced plant growth promotion without affecting bioremediation potential. J Appl Biol Biotechnol, 8:28–34. https://doi.org/10.7324/JABB.2020.80205
Kumar, V., Umrao, P.D. & Kaistha, S.D. (2021). Amelioration of disulfonated acid red and hexavalent chromium phytotoxic effects on triticum aestivum using bioremediating and plant growth-promoting klebsiella pneumoniae sk1. J Pure Appl Microbiol, 15:1301–1312. https://doi.org/10.22207/JPAM.15.3.20
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Mohapatra, R.K., Behera, S.S., Patra, J.K., Thatoi, H. & Parhi, P.K. (2019). Potential application of bacterial biofilm for bioremediation of toxic heavy metals and dye-contaminated environments. New Futur Dev Microb Biotechnol Bioeng Microb Biofilms Curr Res Futur Trends Microb Biofilms, 267–281. https://doi.org/10.1016/B978-0-444-64279-0.00017-7
Mukherjee, P., Roychowdhury, R. & Roy, M. (2017). Phytoremediation potential of rhizobacterial isolates from Kans grass ( Saccharum spontaneumi ) of fly ash ponds. Clean Technol Environ Policy, 19:1373–1385. https://doi.org/10.1007/s10098-017-1336-y
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Roy, S., Sciences, F., Roychowdhury, R. & Zaman, S. (2017). Isolation and characterization of heavy metal resistant and plant growth promoting Staphylococcus sp . from fly ash dump. Int J Adv Res, 5(3):95–103
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Bodor, A., Bounedjoum, N., Vincze, G.E., Erdeiné, Kis. Á., Laczi, K., Bende, G., et al. (2020). Challenges of unculturable bacteria: environmental perspectives. Rev Environ Sci Biotechnol, 19:1–22. https://doi.org/10.1007/s11157-020-09522-4
Melo, P. d. C., Ferreira, L. V., Filho, A. L. M. M., Zafalon, L. F., Vicente, H. I. G. & Souza, V. A. d. (2013). Comparison of methods for the detection of biofilm formation by Staphylococcus aureus isolated from bovine subclinical mastitis. Braz J Microbiol, 44:119–24. https://doi.org/10.1590/S1517-83822013005000031
Desai, C., Jain, K., Patel, B. & Madamwar, D. (2009). Efficacy of bacterial consortium-AIE2 for contemporaneous Cr(VI) and azo dye bioremediation in batch and continuous bioreactor systems, monitoring steady-state bacterial dynamics using qPCR assays. Biodegradation, 20:813–26. https://doi.org/10.1007/s10532-009-9269-8
Gangwar, S. & Singh, V.P. (2011). Indole acetic acid differently changes growth and nitrogen metabolism in Pisum sativum L. seedlings under chromium (VI) phytotoxicity: Implication of oxidative stress. Sci Hortic (Amsterdam), 129:321–328. https://doi.org/10.1016/J.SCIENTA.2011.03.026
Garg, S.K., Tripathi, M. & Srinath, T. (2012). Strategies for chromium bioremediation of tannery effluent. Rev Environ Contam Toxicol, 217:75–140. https://doi.org/10.1007/978-1-4614-2329-4_2
Gianoncelli, A., Zacco, A., Struis, R.P.W.J., Borgese, L., Depero, L.E. & Bontempi, E. (2013). Fly ash Pollutants, treatment and recycling. Springer, Cham, pp 103–213
Holt, J., Krieg, N., Sneath, P., Staley, J. & Williams, S. (1994). Bergey’s Manual of Determinative Bacteriology, 9th edn. Williams and Wilkins, Baltimore, Maryland, USA.
Humphries, R.M., Ambler, J., Mitchell, S.L., Castanheira, M., Dingle, T., Hindler, J.A., et al. (2018). CLSI Methods Development and Standardization Working Group Best Practices for Evaluation of Antimicrobial Susceptibility Tests. J Clin Microbiol, 56:. https://doi.org/10.1128/JCM.01934-17
Hussain, S., Maqbool, Z., Shahid, M., Shahzad, T., Muzammil, S., Zubair, M., et al. (2020). Simultaneous removal of reactive dyes and hexavalent chromium by a metal tolerant Pseudomonas sp. WS-D/183 harboring plant growth promoting traits. Int J Agric Biol, 23:. https://doi.org/10.17957/IJAB/15.1282
Karthik, C. & Arulselvi, P.I. (2017). Biotoxic Effect of Chromium (VI) on Plant Growth-Promoting Traits of Novel Cellulosimicrobium funkei Strain AR8 Isolated from Phaseolus vulgaris Rhizosphere. Geomicrobiol J, 34:434–442. https://doi.org/10.1080/01490451.2016.1219429
Khatoon, Z., Huang, S., Rafique, M., Fakhar, A., Kamran, M.A. & Santoyo, G. (2020). Unlocking the potential of plant growth-promoting rhizobacteria on soil health and the sustainability of agricultural systems. J Environ Manage, 273:111118. https://doi.org/https://doi.org/10.1016/j.jenvman.2020.111118
Kour, D., Kaur, T., Devi, R., Yadav, A., Singh, M., Joshi, D., et al. (2021). Beneficial microbiomes for bioremediation of diverse contaminated environments for environmental sustainability: present status and future challenges. Environ Sci Pollut Res, 28:24917–24939. https://doi.org/10.1007/s11356-021-13252-7
Kumar, Garg S., Tripathi, M., Singh, S.K. & Tiwari, J.K. (2012). Biodecolorization of textile dye effluent by Pseudomonas putida SKG-1 (MTCC 10510) under the conditions optimized for monoazo dye orange II color removal in simulated minimal salt medium. Int Biodeterior Biodegrad, 74:24–35. https://doi.org/10.1016/j.ibiod.2012.07.007
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kumar, V., Omar, R. & Kaistha, S.D. (2016). Phytoremediation Enhanced with Concurrent Microbial Plant Growth Promotion and Hexavalent Chromium Bioreduction. J Bacteriol Mycol Open Access, 2:1–3. https://doi.org/10.15406/jbmoa.2016.02.00045
Kumar, V., Omar, R.A., Umrao, P.D. & Kaistha, S.D. (2020). Cr(VI) toxicity inhibits microbe enhanced plant growth promotion without affecting bioremediation potential. J Appl Biol Biotechnol, 8:28–34. https://doi.org/10.7324/JABB.2020.80205
Kumar, V., Umrao, P.D. & Kaistha, S.D. (2021). Amelioration of disulfonated acid red and hexavalent chromium phytotoxic effects on triticum aestivum using bioremediating and plant growth-promoting klebsiella pneumoniae sk1. J Pure Appl Microbiol, 15:1301–1312. https://doi.org/10.22207/JPAM.15.3.20
Lisa, Evans E. (2011). EPA’s Blind Spot: Hexavalent chromium in coal ash
Lorck, H. (1948). Production of hydrocyanic acid by bacteria. Physiol Plant, 1:142–146. https://doi.org/10.1111/j.1399-3054.1948.tb07118.x
Mishra, S., Chen, S., Saratale, G.D., Saratale, R.G., Romanholo, Ferreira L.F., Bilal, M. et al. (2021). Reduction of hexavalent chromium by Microbacterium paraoxydans isolated from tannery wastewater and characterization of its reduced products. J Water Process Eng, 39:101748. https://doi.org/10.1016/j.jwpe.2020.101748
Mohanty, S. & Patra, N.R. (2015). Geotechnical characterization of Panki and Panipat pond ash in India. Int J Geo-Engineering, 6:13. https://doi.org/10.1186/s40703-015-0013-4
Mohapatra, R.K., Behera, S.S., Patra, J.K., Thatoi, H. & Parhi, P.K. (2019). Potential application of bacterial biofilm for bioremediation of toxic heavy metals and dye-contaminated environments. New Futur Dev Microb Biotechnol Bioeng Microb Biofilms Curr Res Futur Trends Microb Biofilms, 267–281. https://doi.org/10.1016/B978-0-444-64279-0.00017-7
Mukherjee, P., Roychowdhury, R. & Roy, M. (2017). Phytoremediation potential of rhizobacterial isolates from Kans grass ( Saccharum spontaneumi ) of fly ash ponds. Clean Technol Environ Policy, 19:1373–1385. https://doi.org/10.1007/s10098-017-1336-y
Nautiyal, C.S. (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett, 170:265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Ngo, A.C.R. & Tischler, D. (2022). Microbial Degradation of Azo Dyes: Approaches and Prospects for a Hazard-Free Conversion by Microorganisms. Int J Environ Res Public Health, 19:. https://doi.org/10.3390/ijerph19084740
Oliveira, H. (2012). Chromium as an environmental pollutant: insights on induced plant toxicity. J Bot, 2012:1–8. https://doi.org/10.1155/2012/375843
Oves, M., Khan, M.S. & Zaidi, A. (2013). Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur J Soil Biol, 56:72–83. https://doi.org/10.1016/j.ejsobi.2013.02.002
Parveen, S., Bhat, I.U.H., Khanam, Z., Rak, A.E., Yusoff, H.M. & Akhter, M.S. (2022). Phytoremediation: In situ alternative for pollutant removal from contaminated natural media: A brief review. Biointerface Res Appl Chem, 12:4945–4960. https://doi.org/10.33263/BRIAC124.49 454960
Patten, C.L. & Glick, .BR. (1996). Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol, 42:207–220. https://doi.org/10.1139/m96-032
Payne, S.M. (1994). Detection, isolation, and characterization of siderophores. Methods Enzymol, 235:329–344. https://doi.org/10.1016/0076-6879(94)35151-1
Pikovskaya, R. (1948). Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Microbiology, 17:362–370
Qadir, M., Hussain, A., Hamayun, M., Shah, M., Iqbal, A., Husna, et al. (2020). Phytohormones producing rhizobacterium alleviates chromium toxicity in Helianthus annuus L. by reducing chromate uptake and strengthening antioxidant system. Chemosphere, 258:127386. https://doi.org/10.1016/j.chemosphere.2020.127386
Quintelas, C., Fernandes, B., Castro, J., Figueiredo, H. & Tavares, T. (2008). Biosorption of Cr(VI) by a Bacillus coagulans biofilm supported on granular activated carbon (GAC). Chem Eng J, 136:195–203. https://doi.org/10.1016/j.cej.2007.03.082
Roy, S., Sciences, F., Roychowdhury, R. & Zaman, S. (2017). Isolation and characterization of heavy metal resistant and plant growth promoting Staphylococcus sp . from fly ash dump. Int J Adv Res, 5(3):95–103
Sagar, S., Dwivedi, A., Yadav, S., Tripathi, M. & Kaistha, S.D. (2012). Hexavalent chromium reduction and plant growth promotion by Staphylococcus arlettae Strain Cr11. Chemosphere, 86:. https://doi.org/10.1016/j.chemosphe re.2011.11.031
Saini, S., Kaur, N. & Pati, P.K. (2021). Phytohormones: Key players in the modulation of heavy metal stress tolerance in plants. Ecotoxicol Environ Saf, 223:112578. https://doi.org/10.1016/j.ecoenv.2021.112578
Schwyn, B. & Neilands, J.B. (1987). Universal chemical assay for the detection and determination of siderophores. Anal Biochem, 160:47–56
Senapati, M.R. (2011). Fly ash from thermal power plants – waste management and overview. Curr. Sci. 100:1791–1794
Shreya, D., Jinal, H.N., Kartik, V.P. & Amaresan, N. (2020). Amelioration effect of chromium-tolerant bacteria on growth, physiological properties and chromium mobilization in chickpea (Cicer arietinum) under chromium stress. Arch Microbiol, 202:887–894. https://doi.org/10.1007/s00203-019-01801-1
Tahri, Joutey N., Bahafid, W., Sayel, H., Maâtaoui, H., Errachidi, F. & El, Ghachtouli N. (2015). Use of Experimental Factorial Design for Optimization of Hexavalent Chromium Removal by a Bacterial Consortium: Soil Microcosm Bioremediation. Soil Sediment Contam An Int J, 24:129–142. https://doi.org/10.1080/15320 383.2014.92 2931
Thatoi, H.N. & Pradhan, S.K. (2018). Detoxification and bioremediation of hexavalent chromium using microbes and their genes: An insight into genomic, proteomic and bioinformatics studies
Tiwari, S. & Lata, C. (2018). Heavy metal stress, signaling, and tolerance due to plant-associated microbes: An overview. Front Plant Sci, 9:1–12. https://doi.org/10.3389/fpls.2018.00452
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Heavy metal, salinity and azo dye tolerant, Cr (VI) reducing, plant growth-promoting Pseudomonas aeruginosa R32 reverses Cr (VI) biotoxic effects in Vigna mungo. (2023). Journal of Applied and Natural Science, 15(3), 1158-1169. https://doi.org/10.31018/jans.v15i3.4726
