Reducing Pb accumulation in roots of sweet potato under low lead-contaminated soil by Azotobacter inoculation

Authors

  • Reginawanti Hindersah Department of Soil Science, Faculty of Agriculture, Universitas Padjadjaran http://orcid.org/0000-0003-0281-2363
  • Vera Oktavia Subarja Department of Soil Science, Faculty of Agriculture, Karawang University
  • Pujawati Suryatmana Department of Soil Science, Faculty of Agriculture, Universitas Padjadjaran
  • Rija Sudirja Department of Soil Science, Faculty of Agriculture, Universitas Padjadjaran
  • Agung Karuniawan Department of Agronomy, Faculty of Agriculture, Universitas Padjadjaran
  • Yusup Hidayat Department of Plant Pest and Diseases, Faculty of Agriculture, Universitas Padjadjaran

DOI:

https://doi.org/10.15243/jdmlm.2023.102.4271

Keywords:

Azotobacter, biomass, Pb resistance, Pb uptake, soil Pb

Abstract

Agricultural soil is possibly threatened by lead (Pb) contamination due to the intensive use of fertilizers. The rhizobacteria were recommended for the bioremediation of soils contaminated by low concentrations of Pb. The experiment was conducted to observe the Azotobacter's ability to proliferate in Pb-contaminated broth and to decrease the Pb availability in soil, Pb uptake by sweet potato roots, and sweet potato growth. The resistance test was performed by growing five Azotobacter isolates in N-free broth with various Pb levels. A pot experiment was conducted in a factorial randomized block design to test three levels of Pb in soil and two Azotobacter isolates. The results showed that Azotobacter Azv4 and A. choroococcum were resistant to 100 mg L-1 Pb in N-free broth. In the pot experiment, Azotobacter Azv4 Inoculation caused less Pb in soil and roots of sweet potatoes grown in Pb-contaminated soil than A. choroococcum. Either Azotobacter or Pb soil did not influence vine length. However, Azv4 was more prominent in increasing branch number, root volume and length; higher Pb in soil reduced branch number but did not affect root parameters. Azotobacter Azv4 increased more shoot and root dry weight compared to A. choroococcum, but both isolates did not change the shoot-to-root ratio (S/R). The Pb contamination only reduced root dry weight and reduced the S/R. This research considered utilizing rhizobacteria Azotobacter for reducing Pb levels in soil and roots; and increasing sweet potato biomass.

Author Biography

Reginawanti Hindersah, Department of Soil Science, Faculty of Agriculture, Universitas Padjadjaran

Department of Soil Science, Faculty of Agriculture, Padjadjaran University

References

Abedaboohanah, M., Kareem, A., Al-Tufaili, H., Hayder, A., Munem, A.A., Turk, H.A.M. and Abdel-Hassan, N.M. 2020. Effect of adding biofertelizer Azotobacter and foliar spray with nitrogen on growth parameters of potato plant Solanum tuberosum L. cv-Bellini. International Journal of Agricultural and Statistics Sciences 15(2):591-594.

AI-Qasi, B.A., Sharqi, M.M. and Faiath, S.E. 2021. Effect of nitrogen fertilizer sources, lead and cadmium pollution on some properties of barley (Hordeum vulgare). IOP Conference Series: Earth and Environmental Science 904:012057, doi:10.1088/1755-1315/904/1/012057.

Al-Hadi, F., Hussain, F., Hussain, M., Sanaullah, Ahmad, A., Ur Rahman, S. and Ali, A. 2014. Phytoextraction of Pb and Cd; the effect of Urea and EDTA on Cannabis sativa growth under metals stress. International Journal of Agronomy and Agricultural Research 5(3):30-39

Alias, A.A. 2013. Heavy metals in sweet potato and its potential health risk to human. Thesis. Universiti Teknologi MARA, Selangor, Puncak Alam Campus, Faculty of Health Sciences. Available at https://ir.uitm.edu.my/id/eprint/44188/1/44188.PDF

Almaz, M.G., Halim, R.A., Martini, M.Y. and Samsuri, A.W. 2017. Integrated application of poultry manure and chemical fertiliser on soil chemical properties and nutrient uptake of maize and soybean. Malaysian Journal of Soil Science 21:13-28.

Azzi, V., El Samrani, A., Lartiges, B., Kobeissi, A., Kanso, A. and El-Samrani, A.G. 2017. Trace metals in phosphate fertilizers used in eastern Mediterranean Countries. CLEAN - Soil, Air, Water 45(1):1500988, doi:10.1002/clen.201500988.

Ben-David, A. and Davidson, C.E. 2014. Estimation method for serial dilution experiments. Journal of Microbiological Methods 107:214-221, doi:10.1016/j.mimet.2014.08.023.

Benson, N. 2014. Trace metals levels in inorganic fertilizers commercially available in Nigeria. Journal of Scientific Research and Reports 3(4):610-620, doi:10.9734/JSRR/2014/7465.

Dhevagi, P., Priyatharshinis, Ramya, A. and Sudhakaran, M. 2021. Biosorption of lead ions by exopolysaccharide producing Azotobacter sp. Journal of Environmental Biology 42(1):40-50, doi:10.22438/jeb/42/1/MRN-1231.

Gauri, S.S., Mandal, S.M. and Pati, B.R.. 2012. Impact of Azotobacter exopolysaccharides on sustainable agriculture. Applied Microbiology and Biotechnology 95:331-338, doi:10.1007/s00253-012-4159-0,

Hadi, F. and Aziz, T. 2015. A mini review on lead (Pb) toxicity in plants. Journal of Biology and Life Science 6(2):91-101, doi:10.5296/jbls.v6i2.7152

Handleym, H.K., Blichert-Toft, J., Gertisser, R., Macpherson, C.G., Turner, S.P., Zaennudin, A. and Abdurrachman, M. 2014. Insights from Pb and O isotopes into along-arc variations in subduction inputs and crustal assimilation for volcanic rocks in Java, Sunda Arc, Indonesia. Geochimica et Cosmochimica Acta 139:205-226, doi:10.1016/j.gca.2014.04.025.

Hanyabui, E., Apori, S.O., Frimpong, K.A., Atiah, K., Abindaw, T., Ali, M., Asiamah, J.Y. and Byalebeka, J. 2020. Phosphorus sorption in tropical soils. AIMS Agriculture and Food 5(4):599-616, doi:10.3934/agrfood.2020.4.599.

Hindersah, R. 2015. Growth and composition of exopolysaccharides of nitrogen-fixing bacteria Azotobacter spp. on media containing cadmium. Proceedings of the Indonesian Biodiversity National Seminar 1(7):1644-1648, doi:10.13057/psnmbi/m010718 (in Indonesian).

Hindersah, R., Kamaluddin, N.N., Banerjee, S., Sumanta, S. and S. Sarkar. 2020. Role and perspective of Azotobacter in crops production. Sains Tanah-Journal of Soil Science and Agroclimate 17(2):170-179, doi:10.20961/stjssa.v17i2.45130.

Hindersah, R., Karuniawan, A. and Apriliana, A. 2021. Reducing chemical fertilizer in sweet potato cultivation by using mixed biofertilizer. Iraqi Journal of Agricultural Sciences 52(4):1031-1038, doi:10.36103/ijas.v52i4.1414.

Hindersah, R., Mulyani, O. and Osok, R. 2017. Proliferation and exopolysaccharide production of Azotobacter in the presence of mercury. Biodiversity Journal 8(1):21-26.

Holz, M., Zarebanadkouki, M., Kuzyakov, Y., Pausch, Y. and Carminati, A. 2018. Root hairs increase rhizosphere extension and carbon input to soil. Annals of Botany 121(1):61-69, doi:10.1093/aob/mcx127.

Hussien, H. and Ghazi, A.A. 2016. Effect of biomineral fertilization on sweet potato productivity and quality. Proceeding of 1st International Conference of Applied Microbiology pp 21-35, doi:10.21608/mjss.2016.176576.

Jain, S., Muneer, S., Guerriero, G., Liu, S., Vishwakarma, K., Chauhan, D.K., Dubey, N.K., Tripathi, D.K. and Sharma, S. 2018. Tracing the role of plant proteins in the response to metal toxicity: A comprehensive review. Plant Signal Behavior 13(9):e1507401, doi:15592324.2018.1507401.

Jalmi, S.K., Bhagat, P.K., Verma, D., Noryang, S., Tayyeba, S., Singh, K., Sharma, D. and Sinha, A.K. 2018. Traversing the links between heavy metal stress and plant signaling. Frontiers in Plant Science 9:12, doi:10.3389/fpls.2018.00012.

Keran, H., OdobaÅ¡ić, A., Ćatić, S., Salkić, M., BratovÄić, A. and Å estan, I. 2008. The influence of different soil conditions to the lead bioavailability to plants. 12th International Research/Expert Conference on â€Trends in the Development of Machinery and Associated Technologyâ€, Istanbul, Turkey, 26-30 August 2008.

Kratz, S., Schick, J. and Schnug, E. 2016. Trace elements in rock phosphates and P containing mineral and organo-mineral fertilizers sold in Germany. Science of the Total Environment 542:1013-1019, doi:10.1016/j.scitotenv.2015.08.046.

Kuntal Shah, A.U., Mankad, M. and Reddy, N. 2017. Lead accumulation and its effects on growth and biochemical parameters in Tagetes erecta L. International Journal of Life Science and Scientific Research 3(4):1142-1147, doi:10.21276/ijlssr.2017.3.4.7.

Li, N., Liu, J., Yang, R. and Wu, L. 2020. Distribution, characteristics of extracellular polymeric substances of Phanerochaete chrysosporium under lead ion stress and the influence on Pb removal. Scientific Reports 10:17633, doi:10.1038/s41598-020-74983-0.

Liu, H., Li, P., Wang, H., Qing, C., Tan, T., Shi, B., Zhang, G., Jiang, Z., Wang, Y. and Hasan, S.Z. 2020. Arsenic mobilization affected by extracellular polymeric substances (EPS) of the dissimilatory iron-reducing bacteria isolated from high arsenic groundwater. Science of the Total Environment 735(1):139501, doi:10.1016/j.scitotenv.2020.139501.

Luis, G., Rubio, C., Gutiérrez, A.J., González-Weller, D. and Hardisson, C.R.A. 2014. Evaluation of metals in several varieties of sweet potatoes (Ipomoea batatas L.):Comparative study. Environmental Monitoring and Assessment 186(1):433-440, doi:10.1007/s10661-013-3388-8.

Lungu, O.I. and Dynoodt, R.F.P. 2008. Acidification from long-term use of urea and its effect on selected soil properties. African Journal of Food Agriculture Nutrition and Development 8(1):63-76.

Ministry of State for Population and Environment Republic of Indonesia and Dalhousie University Canada. 1992. Environmental Management in Indonesia. Report on Soil Quality Standards for Indonesia (interim report).

Mukhtar, H., Bashir, H. and Nawaz, A. 2018. Optimization of growth conditions for Azotobacter species and their use as biofertilizer. Journal of Bacteriology and Mycology 6(5):274-278, doi:10.15406/jbmoa.2018.06.00217.

Nas, F.S. and Ali, M. 2018. The effect of lead on plants in terms of growing and biochemical parameters: A review. MOJ Ecology and Environmental Science 3(4):265-268, doi:10.15406/mojes.2018.03.00098.

Pembere, A.M.S. 2018. Heavy Metal Levels in Food Crops and Soils from Western Kenya Paperback-16 July 2018. Lambert Academic Publishing. Chisinau, MD-2012, Republic of Moldova. pp 96.

PPT. 1993. Soil Research Center Regulation. Regulation number 59. Soil Research Center, Bogor, Indonesia (in Indonesian).

Prabhakaran, P., Ashraf, M.A., Aqma, W.S. and Noor, W.M. 2016. Microbial stress response to heavy metal in the environment. RSC Advances 6:109862-109877, doi:10.1039/C6RA10966G.

Rasulov, B.A., Yili, A. and Aisa, H.A. 2013. Biosorption of metal ions by exopolysaccharide produced by Azotobacter chroococcum XU1. Journal of Environmental Protection 4(9):989-993, doi:10.4236/jep.2013.49114.

Relente, F.A.C. and Asio, L.G. 2020. Nitrogen application improved the growth and yield performance of sweet potato (Ipomoea batatas (L) Lam.). Annlas of Tropical Research 42(1):45-55, doi:10.32945/atr4214.2020.

Rizvi, A., Ahmed, B., Zaidi, A. and Khan, M.S. 2019. Bioreduction of toxicity influenced by bioactive molecules secreted under metal stress by Azotobacter chroococcum. Ecotoxicity 28(3): 302-322, doi:10.1007/s10646-019-02023-3.

Shetty, P., Acharya, C. and Veeresh, N. 2019. Effect of urea fertilizer on the biochemical characteristics of soil. International Journal of Applied Science and Biotechnology 7(4):414-420, doi:10.3126/ijasbt.v7i4.26778.

Shi, Z., Di Toro, D.M., Allen, H.E and Sparks, D.L. 2013. A general model for kinetics of heavy metal adsorption and desorption on soils. Environmental Science and Technology 47(8):3761-3767, doi:10.1021/es304524p.

Sulaeman, Suparto and Eviati. 2005. Technical Guidelines: Chemical Analysis of Soil, Plants, Water, and Fertilizers. Indonesian Soil Research Institute. 234p ISBN 978-602-8039-21-5 (in Indonesian).

Upadhyay, S.K., Kumar, N., Singh, V. K. and Singh, A. 2015. Isolation, characterization and morphological study of Azotobacter isolates. Journal of Applied and Natural Science 7(2 SE): 984-990, doi:10.31018/jans.v7i2.718.

Upadhyay, S.K., Srivastava, A.K., Rajput, V.D., Chauhan, P.K., Bhojiya, A.A., Jain, D., Chaubey, G., Dwivedi, P., Sharma, B. and Minkina, T. 2022. Root exudates: Mechanistic insight of plant growth promoting rhizobacteria for sustainable crop production. Frontiers in Microbiology 13:916488, doi:10.3389/fmicb.2022.916488.

Van Oosten, M.J., Di Stasio, E., Cirillo, V., Silletti, S., Ventorino, V., Pepe, O., Raimondi, G. and Maggio, A. 2018. Root inoculation with Azotobacter chroococcum 76A enhances tomato plants adaptation to salt stress under low N conditions. BMC Plant Biology 18:205, doi:10.1186/s12870-018-1411-5.

Wei, B., Yu, J., Cao, Z., Meng, M., Yang, L. and Chen, Q. 2020. The availability and accumulation of heavy metals in greenhouse soils associated with intensive fertilizer application. International Journal of Environmental Research and Public Health 17:5359, doi:10.3390/ijerph17155359.

Wierzbowska, J., KovaÄik, P., Sienkiewicz, S., Krzebietke, S. and Bowszys, T. 2018. Determination of heavy metals and their availability to plants in soil fertilized with different waste substances. Environmental and Monitoring Assessment 190:567, doi:10.1007/s10661-018-6941-7.

Williams, L.E., Pittman, J.K. and Hall, J.L. 2000. Emerging mechanisms for heavy metal transport in plants. Biochimica et Biophysica Acta-Biomembranes 1465(1-2):104-126, doi:10.1016/S0005-2736(00)00133-4.

Wu, Y., Li, Z., Yang, Y., Purchase, D., Lu, Y. and Dai Z. 2021. Extracellular polymeric substances facilitate the adsorption and migration of Cu2+ and Cd2+ in saturated porous media. Biomolecules 11(11):1715, doi:10.3390/biom11111715.

Yan, K., Dong, Z., Wijayawardena, M.A.A., Liu, Y. and Naidu, R. 2017. Measurement of soil lead bioavailability and influence of soil types and properties: A review. Chemosphere 184(October):27-42, doi:10.1016/j.chemosphere.2017.05.143.

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Submitted

26-09-2022

Accepted

21-11-2022

Published

01-01-2023

How to Cite

Hindersah, R., Subarja, V. O., Suryatmana, P., Sudirja, R., Karuniawan, A., & Hidayat, Y. (2023). Reducing Pb accumulation in roots of sweet potato under low lead-contaminated soil by Azotobacter inoculation. Journal of Degraded and Mining Lands Management, 10(2), 4271–4280. https://doi.org/10.15243/jdmlm.2023.102.4271

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Research Article

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