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Remediation of Cadmium-Polluted Soil Using Plant Growth-Promoting Rhizobacteria and Natural Zeolite

  • DEGRADATION, REHABILITATION, AND CONSERVATION OF SOILS
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Abstract—

The impact of two strains of Pseudomonas bacteria and natural zeolite on the growth and elemental composition of barley plants was studied in an agrogray soil (Luvisol) artificially contaminated with cadmium in pot experiments. Application of P. fluorescens 21, or P. putida 23, or zeolite eliminated the heavy metal toxicity for plants. The cumulative effect of co-application of P. fluorescens 21 and zeolite was insignificant. The bacteria- or zeolite-mediated plant tolerance to cadmium was attributed to the enhanced root system development, decreased cadmium translocation into the roots, and improved mineral nutrition of the plants. Elevated nutrient uptake by the plants under the influence of bacteria and zeolite was the result of plant growth stimulation without significant changes in the concentrations of macronutrients N, P, K, Ca, and Mg, as well as Fe and micronutrients Zn, Mn, and Cu in plant tissues, including grain. Application of P. fluorescens 21 enhanced the Cd fixation in the soil organic matter in the first half of the growing season, which could be due to the metal sequestration by bacterial siderophores. Thus, application of the bacteria and natural zeolite can be recommended in the strategies for Cd-polluted soil remediation based on environment-friendly technologies.

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REFERENCES

  1. T. O. Anokhina, T. V. Siunova, O. I. Sizova, N. S. Zakharchenko, and V. V. Kochetkov, “Rhizosphere bacteria of genus Pseudomonas in modern agricultural biotechnologies,” Agrokhimiya, No. 10, 54–66 (2018).https://doi.org/10.1134/S0002188118100034

    Article  Google Scholar 

  2. V. S. Barsukova, Physiological and Genetic Aspects of the Plant Tolerance towards Heavy Metals (Institute of Soil Science and Agrochemistry, Novosibirsk, 1997), No. 47.

  3. Yu. N. Vodyanitskii, “Contamination of soils with heavy metals and metalloids and its ecological hazard (analytic review),” Eurasian Soil Sci. 46, 793–801 (2013).

    Article  Google Scholar 

  4. V. B. Il’in, Heavy Metals and Nonmetals in the Soil–Plant System (Nauka, Novosibirsk, 2012) [in Russian].

    Google Scholar 

  5. N. M. Kaznina and A. F. Titov, “The influence of cadmium on physiological processes and productivity of Poaceae plants,” Biol. Bull. Rev. 4, 335–348 (2014).

    Article  Google Scholar 

  6. A.V. Lednev and A.V. Lozhkin, “Remediation of agrosoddy-podzolic soils contaminated with cadmium,” Eurasian Soil Sci. 50, 620–629 (2017).

    Article  Google Scholar 

  7. V. V. Matichenkov, E. A. Bocharnikova, A. A. Kosobryukhov, and K. Ya. Biel, “Mobile forms of silicon in plants,” Dokl. Biol. Sci. 418, 39–40 (2008).

    Article  Google Scholar 

  8. V. G. Mineev, O. S. Safrina, and V. P. Shabayev, “Effect of bacteria of genus Pseudomonas on some physiological-biochemical processes in the Beta vulgaris plants,” Dokl. Vses. Akad. S-kh. Nauk im. V.I. Lenina, No. 1, 16–21 (1992).

    Google Scholar 

  9. T. M. Minkina, G. V. Motuzova, and O. G. Nazarenko, The Composition of Heavy Metals in Soils (Everest, Rostov-on-Don, 2009) [in Russian].

    Google Scholar 

  10. A. V. Nazarov and S. A. Ilarionov, “Potential use of microbial-plant interaction for bioremediation,” Biotekhnologiya, No. 5, 58–62 (2005).

    Google Scholar 

  11. G. A. Romanov, Zeolites: Efficiency and Application in Agriculture (Rosinformagrotekh, Moscow, 2000) [in Russian].

    Google Scholar 

  12. M. G. Sokolova, G. A. Belogolova, G. P. Akimova, and O. B. Vaishlya, “Effect of inoculation by rhizosphere bacteria on growth of the plants and translocation of trace elements in polluted soils,” Agrokhimiya, No. 7, 72–80 (2016).

    Google Scholar 

  13. Theory and Practice of the Chemical Analysis of Soils, Ed. by L. A. Vorob’eva (GEOS, Moscow, 2006), pp. 295–296.

    Google Scholar 

  14. A. F. Titov, V. V. Talanova, N. M. Kaznina, and G. F. Laidinen, The Plant Tolerance towards Heavy Metals (Karelian Scientific Center, Russian Academy of Sciences, Petrozavodsk, 2007) [in Russian].

    Google Scholar 

  15. V. P. Shabaev, “Soil-agrochemical aspects of remediation of a gray forest soil polluted with Pb upon the application of growth-promoting rhizobacteria,” Eurasian Soil Sci. 45, 539–549 (2012).

    Article  Google Scholar 

  16. O. H. Ahmed, G. Sumalatha, and A. N. Muhamad, “Use of zeolite in maize (Zea mays) cultivation on nitrogen, potassium and phosphorus uptake and use efficiency,” Int. J. Phys. Sci. 5 (15), 2393–2401 (2010).

    Google Scholar 

  17. T. Balakhnina, P. Bulak, V. Matichenkov, A. Kosobryukhov, and T. Wlodarczyk, “The influence of Si-rich mineral zeolite on the growth processes and adaptive potential of barley plants under cadmium stress,” Plant Growth Regul. 75 (2), 557–565 (2015). https://doi.org/10.1007/s10725-014-0021-y

    Article  Google Scholar 

  18. A. C. Campos Bernardi, P. P. A. Oliviera, M. B. de Melo Monte, and F. Souza-Barros, “Brazilian sedimentary zeolite use in agriculture,” Microporous Mesoporous Mater. 16, 16–21 (2013). https://doi.org/10.1016/j.micromeso.2012.06.051

    Article  Google Scholar 

  19. S. Clemens, “Molecular mechanisms of plant metal tolerance and homeostasis,” Planta 212 (4), 475–486 (2001). https://doi.org/10.1007/s004250000458

    Article  Google Scholar 

  20. M. S. Cortese, A. Paszczynski, T. A. Lewis, J. L. Sebat, V. Borek, and R. L. Crawford, “Metal chelating properties of pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas spp. and the biological activities of the formed complexes,” Biometals 15 (2), 103–120 (2002). https://doi.org/10.1023/A:1015241925322

    Article  Google Scholar 

  21. F. Damian, G. Damian, R. Lacatusu, C. Postolache, G. Iepure, M. Jelea, and D. Nasui, “The heavy metals immobilization in polluted soils from Romania by the natural zeolites use,” Carpathian J. Earth Environ. Sci. 8 (4), 231–250 (2013).

    Google Scholar 

  22. S. Dorjey, D. Dolkar, and R. Sharma, “Plant growth promoting rhizobacteria Pseudomonas: a review,” Int. J. Curr. Microbial. App. Sci. 6 (7), 1335–1344 (2017). https://doi.org/10.20546/ijcmas.2017.602.160

    Article  Google Scholar 

  23. V. Ganesan, “Rhizoremediation of cadmium soil using a cadmium-resistant plant growth-promoting rhizopseudomonad,” Curr. Microbiol. 56 (4), 403–407 (2008). https://doi.org/10.1007/s00284-008-9099-7

    Article  Google Scholar 

  24. M. Hamidpour, M. Afyuni, M. Kalbasi, A. Khoshgoftarmanes, and V. Inglezaki, “Mobility and plant-availability of Cd(II) and Pb(II) adsorbed on zeolite and bentonite,” Appl. Clay Sci. 48 (3), 342–348 (2010). https://doi.org/10.1016/j.clay.2010.01.004

    Article  Google Scholar 

  25. A. Handsa, V. Kumar, Anshumali, and Z. Usmani, “Phytoremediation of heavy metals contaminated soil using plant growth promoting rhizobacteria (PGPR): a current perspective,” Recent Res. Sci. Technol. 6 (1), 131–134 (2014).

    Google Scholar 

  26. P. Jali, C. Pradhan, and A. B. Das, “Effects of cadmium toxicity in plants: a review article,” Scholars Acad. J. Biosci. 4 (12), 1074–1081 (2016). https://doi.org/10.21276/sajb.2016.4.12.3

    Article  Google Scholar 

  27. X. Ji, S. Liu, J. Huang, E. Bocharnikova, and V. Matichenkov, “Monosilicic acid potential in phytoremediation of the contaminated areas,” Chemosphere 157, 132–136 (2016). https://doi.org/10.1016/j.chemosphere.2016.05.029

    Article  Google Scholar 

  28. X. Ji, S. Liu, P. Hua, E. A. Bocharnikova, V. V. Matychenkov, and D. M. Khomyakov, “Cadmium and arsenic adsorption in aqueous systems in the presence of monosilicic acid,” Moscow Univ. Soil Sci. Bull. 72 (5), 199–206 (2017). https://doi.org/10.3103/S0147687417050040

    Article  Google Scholar 

  29. X. Ji, S. Liu, H. Juan, E. Bocharnikova, and V. Matichenkov, “Effect of silicon fertilizers on cadmium in rice (Oryza sativa) tissue at tillering stage,” Environ. Sci. Pollut. Res. 24 (11), 10740–10748 (2017). https://doi.org/10.1007/s11356-017-8730-1

    Article  Google Scholar 

  30. A. Kabata-Pendias, Trace Elements in Soils and Plants (CRC Press, Boca Raton, 2011).

    Google Scholar 

  31. M. S. Khan, A. Zaidi, P. A. Wani, and M. Oves, “Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils,” Environ. Chem. Lett. 7 (1), 1–19 (2009). https://doi.org/10.1007/s10311-011-0338-y

    Article  Google Scholar 

  32. T. Lebeau, A. Braud, and K. Jézéquel, “Performance of bioaugmentation assisted phytoextraction applied to metal contaminated soils: a review,” Environ. Pollut. 153 (3), 497–522 (2008). https://doi.org/10.1016/j.envpol.2007.09.015

    Article  Google Scholar 

  33. V. V. Matichenkov, X. Wei, D. Liu, and E. A. Bocharnikova, “Theory, practice and prospection of Si fertilizer,” Agric. Sci. Technol. 14 (3), 498–502 (2013).

    Google Scholar 

  34. A. Meliani and A. Bensoltane, “Biofilm-mediated heavy metals bioremediation in PGPR Pseudomonas,” J. Bioremed. Biodegrad. 7 (5), 370 (2016). https://doi.org/10.4172/2155-6199.1000370

    Article  Google Scholar 

  35. J. Mishra, R. Singh, and N. K. Arora, “Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms,” Front. Microbiol. 8, 1706 (2017). https://doi.org/10.3389/fmicb.2017.01706

    Article  Google Scholar 

  36. H. Mohsen, H. Shirani, and L. Akbari, “Effects of co-application of zeolites and vermicompost on speciation and phytoavailability of cadmium, lead, and zinc in a contaminated soil,” Commun. Soil Sci. Plant Anal. 8 (3), 262–273 (2017). https://doi.org/10.1080/00103624.2016.1261885

    Article  Google Scholar 

  37. G. Muhlbachova and T. Simon, “Effects of zeolite amendment on microbial biomass and respiratory activity in heavy metal contaminated soils,” Plant Soil Environ. 49 (12), 536–541 (2003). https://doi.org/10.17221/4190-PSE

    Article  Google Scholar 

  38. Z. Saeed, M. Naveed, M. Imran, M. A. Bashir, A. Sattar, and A. Mustafa, “Combined use of Enterobacter sp. MN17 and zeolite reverts the adverse effects of cadmium on growth, physiology and antioxidant activity of Brassica napus,” PLoS One 14 (3), (2019). https://doi.org/10.1371/journal.pone.0213016

  39. C. Treesubsuntorn, P. Dhurakit, G. Khaksar, and P. Thiravetyan, “Effect of microorganisms on reducing cadmium uptake and toxicity in rice (Oryza sativa L.),” Environ. Sci. Pollut. Res. 25 (26), 25690–25701 (2018). https://doi.org/10.1007/s11356-017-9058-6

    Article  Google Scholar 

  40. M. Vaculík, A. Lux, M. Luxová, E. Tanimoto, and I. Lichtscheidl, “Silicon mitigates cadmium inhibitory effects in young maize plants,” Environ. Exp. Bot. 67, 52–58 (2009). https://doi.org/10.1016/j.envexpbot.2009.06.012

    Article  Google Scholar 

  41. X. Wei, Y. Liu, Q. Zhan, P. Zhang, D. Zhao, B. Xu, E. Bocharnikova, and V. Matichenkov, “Effect of Si soil amendments on As, Cd, and Pb bioavailability in contaminated paddy soils,” Paddy Water Environ. 16 (1), 173–181 (2018). https://doi.org/10.1007/s10333-017-0629-4

    Article  Google Scholar 

  42. A. M. Zawadzka, A. J. Paszczynski, and R. L. Crawford, “Transformations of toxic metals and metalloids by Pseudomonas stutzeri strain KC and its siderophore pyridine-2,6-bis (thiocarboxylic acid),” in Advances in Applied Bioremediation, Ed. by A. Singh, R. C. Kuhad, and O. P. Ward (Springer-Verlag, Berlin, 2009), pp. 221–238. https://doi.org/10.1007/978-3-540-89621-0_12

    Google Scholar 

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Funding

This study was performed within the framework of state assignment, project nos. AAAA-A18-118013190180-9, AAAA-A17-117030110139-9, and AAAA-A18-118013190181-6.

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Authors and Affiliations

  1. Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, 142290, Pushchino, Moscow oblast, Russia

    V. P. Shabayev & V. E. Ostroumov

  2. Institute of Basic Biological Problems, Russian Academy of Sciences, 142290, Pushchino, Moscow oblast, Russia

    E. A. Bocharnikova

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  1. V. P. Shabayev
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  2. E. A. Bocharnikova
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Correspondence to E. A. Bocharnikova.

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Translated by D. Konyushkov

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Shabayev, V.P., Bocharnikova, E.A. & Ostroumov, V.E. Remediation of Cadmium-Polluted Soil Using Plant Growth-Promoting Rhizobacteria and Natural Zeolite. Eurasian Soil Sc. 53, 809–819 (2020). https://doi.org/10.1134/S1064229320060113

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