Effect of Plant Growth Promoting Rhizobacteria (PGPR) Inoculation on Arsenic Uptake by Sunflower, Corn and Pumpkin in Contaminated Soil

Document Type : Original Article

Authors

1 faculty Member

2 Former MSc. student

3 Faculty member

10.30466/asr.2025.54607.1810

Abstract

Remediation of heavy metals from soil through phytoremediation is considered one of the most cost-effective and environmentally friendly methods. In many cases, beneficial soil microorganisms are utilized to enhance the extraction of heavy metals. In this research, 15 bacteria resistant to arsenic were isolated from the rhizosphere of six native plants around the Sarcheshmeh copper mine in Rafsanjan. According to minimum inhibitory concentration tests of arsenic,it was found that all isolates were resistant to 150 mg L-1 of arsenic and about 70 percent of them were able to grow at a concentration of 500 mg.L-1 of arsenic. Among the arsenic resistant isolates, eight were capable of producing siderophore in the CAS-agar medium and while five were able to produce hydrogen cyanide. Additionally all isolates demonstrated the ability to produce IAA and solubilize insoluble phosphorus compounds in the liquid medium. To evaluate the effect of these isolates on arsenic uptake by plant, three arsenic-resistant isolates with growth-stimulating characteristics were selected for a greenhouse experiment as factorial based on a completely randomized design with four replications. The tested factors included three levels of plant (sunflower, corn and pumpkin) and bacteria in four levels (non-inoculation, inoculation with BH6, BH9 and BH10 isolates). The results of the greenhouse experiments revealed that the highest  arsenic uptake (77.8 µg pot-1) was observed  in the interaction between the BH9 isolate and pumpkin, representing a 62.1 percent compared to the control. Furthermore, the highest transfer factor (TF) of arsenic was obtained from the interaction of BH9 isolate with pumpkin (0.825), significantly  differing from other treatments. In general, pumpkin and corn plants due to their higher biomass production were more effective in extracting arsenic from the soil, compared to sunflower. The P9 isolate demonstrated the highest efficiency among all isolates tested.

Keywords

Main Subjects


Ahmad F., Ahmad I., and Sahir khan M. 2005. Indole acetic acid production by the indigenous isolates of the Azotobacter and Fluorescent pseudomonads in the presence and absence of tryptophan. Turkish Journal of Biology, 29: 29-34.
Alexander D.B., and Zuberer D.A. 1991. Use of cgrome azural S reagents to evaluate sidrophore production by rhizosphere bacteria. Biology and Fertility of Soils, 12: 39-45.
Alloway B.J. 1995. heavy metals in soils. Blackie Academic and Professional, Chapman and Hall. London, 368p.
Alka  S., Shahir S., Ibrahim N., Ndejiko M .J., Vo D., and Manan F.A. 2021. Arsenic removal technologies and future trends: A mini review. Journal of Cleaner Productio, 276: 1-14.
Baroni F., Boscagli A., Protano G., and Riccobono F. 2000. Antimony accumulation in Achillea ageratum, Plantago lanceolata and Silene vulgaris growing in an old Sb-mining area. Environmental Pollution, 109: 347- 352.
Bent E., Tuzan S., Chanway C.P., and Enebak S. 2001. Alteration in plant growth and in root hormone levels of lodgepole pines inoculated with rhizobacteria. Canadian Journal of Microbiology, 47: 793-800.
Burd G.I., Dixon D.G., and Glick B.R. 2000. Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Canadian Journal of Microbiology, 46: 237- 245.
Chen Y.F. 1994. Review of the research on heavy metal contamination of China’s city soil and its treatment method. Resources and Environment, 21(3): 536-539.
De Maria S., Rivelli A.R., Kuffner M., Sessitsch A., Wenzel W.W., Gorfer M., Strauss  J., and Puschenreiter, M. 2011. Interactions between accumulation of trace elements and major nutrients in Salix caprea after inoculation with rhizosphere microorganisms. Chemosphere, 84: 1256-1261
Donate-Correa J., Leon-Barrios M. and Perez-Galdona R. 2004. Screening for plant growth-promoting rhizobacteria in Chamaecytisus proliferus (tagasaste), a forage treeshrub legume endemic to the Canary Island. Plant Soil, 266: 261-272.
Ellis R.J., Hanway J.J., Holmgren G., Keeney D.R., and Bidwell O.W. 1920. Sampling and Analysis of Soils, Plants, Waste Waters, and Sludge-Suggested Standardization and Methodology. Agricultural Exp. Station, Kansas State University, Manhattan. 230p.
Erfanmanesh M., and Afyuni M. 2012. Environment Pollution Water, Soil and air. Arkan Publication. Esfahan, 318p. (In Persian)
Estefan G., Sommer R., and Ryan J. 2013. Methods of soil, plant and water analysis: A manual for the West Asia and North Africa Region. Beirut: ICARDA.
Grichko V.P., Filby B. and Glick B.R. 2000. Increased ability of transgenic plants expressing the bacterial enzyme ACC-deaminase to accumulate Cd, Co, Cu, Ni, Pb and Zn. Journal of Biotechnology,  81(1): 45-53.
Haghi M., Diznabi S. H., Karaboz I. and Ersoy-Omeroglu E. 2013. Arsenic pollution and arsenic-resistant bacteria of drying Urmia Salt Lake. Frontiers in Environmental Science. 11: 1195643 
Hamidpour M., Afyuni M., Kalbasi M., Khoshgoftarmanes H., and Inglezakis V. J. 2010. Mobility and plant- availability of Cd(II) and Pb(II) adsorbed on zeolite and bentonite. Applied Clay Sciences, 48:342–48.
Hamidpour M., Nemati H. and Abbaszadeh Dahaji P. 2020. Effects of plant growth-promoting bacteria on EDTA-assisted phytostabilization of heavy metals in a contaminated calcareous soil. Environ Geochem Health, 42: 2535–2545 .
Hasani G., Akhgar A., and Tajabadipour A. 2012. Effectiveness of IAA and ACC-deaminase Producing Fluorescent Pseudomonads on Growth of Pistachio Seedlings. Iranian journal of soil science, 26(1): 89-97 (In Persian)
Heidarpour N., Ghasemi Mobtaker H., and Toushih V. 2016. Effects of different tillage methods on dryland wheat yield and soil physical properties in wheat – fallow rotation in Kurdistan. Journal of Soil Management and Sustainable Production, 5(4): 61-77 (In Persian)
Haydarpoor L., Soltani Toolarood A. A. and Goli Kalanpa E. (2017). Evaluation of plant growth promoting traits of arsenic resistant bacteria and their effect on morphological properties of  Origanum vulgare plant in an arsenic-polluted soil. Journal of Soil Biology, 4(2): 135-151(In Persian)
Haydarpoor L., Soltani Toolarood A., and Goli Kalanpa E. 2017. Effect of Arsenic-Resistant Plant Growth Promoting (PGP) Isolates on some Physiological Characteristics, Growth and Nutrition of Mentha peparata L. in an Arsenic-Polluted Soil. Applied Soil Research, 4(2): 14-25
Jiang Y., Lei M., Duan L., Longhurst P. 2015. Integrating phytoremediation with biomass valorisation and critical element recovery: A UK contaminated land perspective. Biomass Bioenergy, 83: 328–339.
Noughi Hojjat F., Akhgar A., Esfandiarpour I., and Khavazi K. 2014. Evaluation of Population and Properties of PGPB of Endorhizosphere, Rhizosphere and Nonrhizosphere in Pistachio Seedlings. Water and Soil Science, 23(4): 215-233 (In Persian)
Karimi A., Khodaverdiloo H., and Rasouli-Sadaghiani M.H. 2018. Microbial-enhanced phytoremediation of lead contaminated calcareous soil by Centaurea cyanus L. Clean–Soil, Air, Water, 46(2), 1700665.
Khaden Moghadam N.,and  GOLCHIN A.  2019. Risk Assessment of Contamination of the Country's Soil and Water Resources with Arsenic. Iranian Journal of Soil and Water Research, 50(7): 1612-1617 (In Persian)
Kirkham M.B., 2006. Cadmium in plants on polluted soils: Effects of soil factors, hyperaccumulation, and amendments. Geoderma, 137: 19-32
Kremer R.J., and Souissi T. 2011. Cyanide production by rhizobacteria and potential for suppression of weed seedlind growth. Current Microbial,  43:182-186
Kloepper J.W. and Schroth M.N. 2008. Plant growth-promoting rhizobacteria on radishes. International Conferencee on plant Pathogenic Bacteria. Tours, 879–882
Ma L.Q., Komar K.M., Tu C., Zhang W., Cai Y., and Kennelley E.D. 2001. A fern that hyperaccumulates arsenic. Nature, 409: 579-582
Maghami M., Olamaee M., Rasuli Sadaghiani M.H., and Dordipour E. 2013. Isolation and identification of Pseudomonas Fluorecens and evaluation of their plant growth promoting properties in soils Golestan province. Journal of Soil Management and Sustainable Production, 3(2): 251-264 (In Persian)
Mawia A.M., Hui S., Zhou L., Li H., Tabassum J., Lai C., Wang J., Shao G., Wei X., Tang S., Luo J., Hu S., and Hu P. 2020. Inorganic arsenic toxicity and alleviation strategies in rice. Journal of Hazard Mater, 408: 1-21
Mendez M.O., and Maier R.M. 2008. Phytostabilization of mine tailings in arid and semiarid environments-an emerging remediation technology. Environmental Health Perspective, 116: 278–283.
Mirzaie N., Reyhanitabar A., Oustan S., and Hagighat Afshar M. 2014. Effects of combined application of as and P on the growth characteristics and uptake of as and P by two wheat and marigold plants. Iranian journal of soil and water research, 45(3): 353-367. (In Persian)
Mosaferi M., and Mesdaghinia A.R. 2005. Removal of Arsenic from drinking water using modified activated alumina. Journal of water and wastewater, 16 (54): 2-14.
Nasirzadeh A., Hamidpour M., Abbaszadeh-Dahaji P., Akhgar, A. and Kariman K. 2023. Zinc-solubilizing Pseudomonas strains improve zinc nutrition of maize plants grown in sand amended with tire waste powder. Journal of Plant Nutrition, 46(14): 3450–3468 .
Penrose M. and Glick B.R. 2003. Methods for isolating and characterizing Acc deaminase- containing Plant Groeth- Promoting Rizobacteria. Physiology Plant, 118: 10-15.
Piracha M.A., Ashraf M. and Niaz A. 2019. Arsenic fractionation and its impact on physiological behavior of sunflower (Helianthus annuus L.) in three texturally different soils under alkaline calcareous conditions. Environmental Science and Pollution Research, 26: 17438–17449.
Rahmanian M., Khodaverdiloo H., Rezaei Danesh Y., and Rasouli Sadaghiani M. 2011. Effects of heavy matal resistant soil microbs inoculation and soil Cd concentration on growth and metal uptake of millet, couch grass and alfalfa. Journal Microbiology Research, 5(4): 403-410
Rajaee S., Alikhani H.A., and Raiesi F. 2007. Effect of Plant Growth Promoting Potentials of Azotobacter chroococcum Native Strains on Growth, Yield and Uptake of Nutrients in Wheat. Journal of Water and Soil Science, 11: 285-297 (In Persian)
Rasouli-Sadaghiani M.H., Barin M., Khodaverdiloo H., Siavash Moghaddam S., Damalas C. A., and Kazemalilou S. 2019. Arbuscular mycorrhizal fungi and rhizobacteria promote growth of Russian knapweed (Acroptilon repens L.) in a Cd-contaminated soil. Journal of Plant Growth Regulation38: 113-121 (In Persian)
Saha D., and Sahu S. 2016.  A decade of investigations on groundwater arsenic contamination in Middle Ganga Plain, India. Environmental geochemistry and health, 38: 315–337.
Sarcheshmepour M., Savaghebi G.h., Saleh Rastin N., Alikhani H., and Pour-Babaei A. 2010. Isolation, screening, identification and determination of relative tolerance to salinity and drought superior strains of bacteria in the rhizosphere growth (PGPR) of pistachio trees. Iranian Journal of Soil and Water Research, 40(2): 177-190 (In Persian)
Sheng X.F., and Xia J.J. 2008. Improvement of rape Brassica napus plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere, 64: 1036–1042.
Smith S.E. and Read D.J. 1997. Mycorrhizal symbiosis. Academic Press, London, 27: 555-561
Sperber J.I. 1958. The incidence of apatite soulbilizing organisms in the rhizospher. Australia Journal Agriculture Research, 9: 778-781.
Srivastava S., Srivastava A. K., Suprasanna P. and D’Souza S. F. 2009. Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. Journal of Experimental Botany, 60: 3419–3431.
Titah, H. S., Abdullah S. R., Idris M., Anuar N., Basri H., Mukhlisin M., Tangahu B. V. Purwanti I. F. and Kurniawan S. B.  2018. Arsenic resistance and biosorption by isolated rhizobacteria from the roots of Ludwigia octovalvis. International Journal of Microbiology, 3101498
Sundra B., Natarajam V. and Hari K. 2002. Influence of phosphorus solubilizing bacteria on the changes in soil available phosphorus and sugarcane and sugar yields. Field Crops Research, 77:43-49.
Wu S.C., Cao Z.H., Li Z.G., Cheung K.C. and Wong M.H. 2005. Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma, 125: 155-166.
Yan-de J., Zhen-li H., and Xiao Y. 2007. Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. Journal of Zhejiang Univercity Science, 8(3): 197- 207.