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http://dx.doi.org/10.4014/jmb.1712.12038

Isolation and Characterization of Pb-Solubilizing Bacteria and Their Effects on Pb Uptake by Brassica juncea: Implications for Microbe-Assisted Phytoremediation  

Yahaghi, Zahra (Department of Soil Science, College of Agriculture, Isfahan University of Technology)
Shirvani, Mehran (Department of Soil Science, College of Agriculture, Isfahan University of Technology)
Nourbakhsh, Farshid (Department of Soil Science, College of Agriculture, Isfahan University of Technology)
de la Pena, Teodoro Coba (Institute of Agricultural Sciences ICA-CSIC)
Pueyo, Jose J. (Institute of Agricultural Sciences ICA-CSIC)
Talebi, Majid (Department of Agricultural Biotechnology, College of Agriculture, Isfahan University of Technology)
Publication Information
Journal of Microbiology and Biotechnology / v.28, no.7, 2018 , pp. 1156-1167 More about this Journal
Abstract
The aim of this study was to isolate and characterize lead (Pb)-solubilizing bacteria from heavy metal-contaminated mine soils and to evaluate their inoculation effects on the growth and Pb absorption of Brassica juncea. The isolates were also evaluated for their plant growth-promoting characteristics as well as heavy metal and salt tolerance. A total of 171 Pb-tolerant isolates were identified, of which only 15 bacterial strains were able to produce clear haloes in solid medium containing PbO or $PbCO_3$, indicating Pb solubilization. All of these 15 strains were also able to dissolve the Pb minerals in a liquid medium, which was accompanied by significant decreases in pH values of the medium. Based on 16S rRNA gene sequence analysis, the Pb-solubilizing strains belonged to genera Bacillus, Paenibacillus, Brevibacterium, and Staphylococcus. A majority of the Pb-solubilizing strains were able to produce indole acetic acid and siderophores to different extents. Two of the Pb-solubilizing isolates were able to solubilize inorganic phosphate as well. Some of the strains displayed tolerance to different heavy metals and to salt stress and were able to grow in a wide pH range. Inoculation with two selected Pb-solubilizing and plant growth-promoting strains, (i.e., Brevibacterium frigoritolerans YSP40 and Bacillus paralicheniformis YSP151) and their consortium enhanced the growth and Pb uptake of B. juncea plants grown in a metal-contaminated soil. The bacterial strains isolated in this study are promising candidates to develop novel microbe-assisted phytoremediation strategies for metal-contaminated soils.
Keywords
Metal-solubilizing bacteria; lead; PGPR; contaminated soils; phytoremediation;
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1 Lindsay WL, Norvell WA. 1978. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci. Soc. Am. J. 42: 421-428.   DOI
2 Mergeau MD, Nies HG, Schlegel J, Gerits P, Charles van Gijsegem F. 1985. Alcaligenes eutrophus CH34 is a facultative chemolitotroph with plasmid-bound resistance to heavy metals. J. Bacteriol. 162: 328-334.   DOI
3 Gordon SA, Weber RP. 1951. Colorimetric estimation of indole acetic acid. Plant Physiol. 26: 192-195.   DOI
4 Alexander DB, Zuberer DA. 1991. Use of chrome Azurol-S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soils 12: 39-45.   DOI
5 Zaidi S, Usmani S, Singh BR, Musarrat J. 2006. Significance of Bacillus subtilis strain SJ-101 as a bio inoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64: 991-997.   DOI
6 Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173: 697-703.   DOI
7 Affan QA, Shoeb E, Badar U, Akhtar J. 2009. Isolation and characterization of bacterial isolates having heavy metal tolerance. J. Basic Appl. Sci. 5: 55-60.
8 Nonnoi F, Chinnaswamy A, de la Torre VSG, de la Pena TC, Lucas MM, Pueyo JJ. 2012. Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercurycontaminated soils. Appl. Soil Ecol. 61: 49-59.   DOI
9 Jones JB Jr, Case VW. 1990. Sampling, handling, and analyzing plant tissue samples, pp. 389-447. In Westerman RL (ed.), Soil Testing and Plant Analysis. Soil Science Society of America, Inc., Madison, WI.
10 NYS. 2006. New York State Brownfield Cleanup Program Development of Soil Cleanup Objectives Technical Support Document. New York State Department of Environmental Conservation and New York State Department of Health, Albany, NY. Available from http://www.dec.ny.gov/chemical/34189.html.
11 Davies PJ. 2010. The Plant Hormones: Their Nature, Occurrence and Functions, 3rd Ed. Kluwer Academic Publishers, New York.
12 Ji LY, Zhang WW, Yu D, Cao YR, Xu H. 2012. Effect of heavy metal-solubilizing microorganisms on zinc and cadmium extractions from heavy metal contaminated soil with Tricholoma lobynsis. World J. Microbiol. Biotechnol. 28: 293-301.   DOI
13 Malhotra M, Srivastava S. 2009. Stress-responsive indole-3-acetic acid biosynthesis by Azospirillum brasilense SM and i ts ability to modulate plant growth. Eur. J. Soil Biol. 45: 73-80.   DOI
14 Patten CL, Glick BR. 2002. The role of bacterial indole acetic acid in the development of the host plant root system. Appl. Environ. Microbiol. 68: 3795-3801.   DOI
15 Ribeiro CM, Cardoso EJBN. 2012. Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol. Res. 167: 69-78.   DOI
16 Rajkumar M, Ae N, Narasimha M, Prasad V, Freitas H. 2009. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28: 142-149.
17 Dimkpa CO, Merten D, Svatos A, Buchel G, Kothe E. 2009. Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol. Biochem. 41: 154-162.   DOI
18 Gao Y, Miao C, Mao L, Zhou P, Jin Z, Shi W. 2010. Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. J. Hazard. Mater. 181: 771-777.   DOI
19 Abou-Shanab RA, Ghozlan H, Ghanem K, Moawad H. 2005. Behavior of bacterial populations isolated from rhizosphere of Diplachne fusca dominant in industrial sites. World J. Microbiol. Biotechnol. 21: 1095-1101.   DOI
20 Li WC, Ye ZH, Wong MH. 2010. Metal mobilization and production of short-chain organic acids by rhizosphere bacteria associated with a Cd/Zn hyperaccumulating plant, Sedum alfredii. Plant Soil 326: 453-467.   DOI
21 Ma Y, Prasad MNV, Rajkumar M, Freitas H. 2011. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol. Adv. 29: 248-258.   DOI
22 Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, et al. 2013. The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol. Biochem. 60: 182-194.   DOI
23 Abou-Shanab RA, Ghanem K, Ghanem N, Al-Kolaibe A. 2008. The role of bacteria on heavy-metal extraction and uptake by plants growing on multi-metal-contaminated soils. World J. Microbiol. Biotechnol. 24: 253-262.   DOI
24 Braud A, Jezequel K, Bazot S, Lebeau T. 2009. Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74: 280-286.   DOI
25 Dimkpa CO, Merten D, Svatos A, Buchel G, Kothe E. 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. Appl. Microbiol. 107: 1687-1696.   DOI
26 Dhal B, Thatoi H, Das N, Pandey BD. 2010. Reduction of hexavalent chromium by Bacillus sp. isolated from chromite mine soils and characterization of reduced product. J. Chem. Technol. Biotechnol. 85: 1471-1479.
27 Govarthanan M, Lee KJ, Cho M, Kim JS, Kamala-Kannan S, Oh BT. 2013. Significance of autochthonous Bacillus sp. KK1 on biomineralization of lead in mine tailings. Chemosphere 90: 2267-2272.   DOI
28 Teixeira C, Almeida CMR, Nunes da Silva M, Bordalo AA, Mucha AP. 2014. Development of autochthonous microbial consortia for enhanced phytoremediation of salt-marsh sediments contaminated with cadmium. Sci. Total Environ. 493: 757-765.   DOI
29 Seralathan K, Kui JL. 2008. Metal tolerance and antibiotic resistance of Bacillus species isolated from Sunchon Bay, South Korea. Biotechnology 7: 149-152.   DOI
30 Sheng XF, He LY, Wang QY, Ye HS, Jiang CY. 2008. Effects of inoculation of biosurfactant-producing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil. J. Hazard. Mater. 155: 17-22.   DOI
31 Kumar KV, Singh N, Behl NH, Srivastava S. 2008. Influence of plant growth promoting bacteria and its mutant on heavy metal toxicity in Brassica juncea grown in fly ash amended soil. Chemosphere 72: 678-683.   DOI
32 Tangahu BV, Abdullah SRS, Basri H, Idris M, Anuar N, Mukhlisin MA. 2011. Review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int. J. Chem. Eng. 2011: 939161.
33 Kumari B, Singh SN. 2011. Phytoremediation of metals from fly ash through bacterial augmentation. Ecotoxicology 20: 166-176.   DOI
34 Burd GI, Dixon DG, Glick BR. 1998. A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol. 64: 3663-3668.
35 Shao HB, Chu LY, Ni FT, Guo DG, Li H, Li WX. 2010. Perspective on phytoremediation for improving heavy metal-contaminated soils, pp. 227-244. In Ashraf M, Ozturk M, Ahmad MSA (eds.), Plant Adaptation and Phytoremediation. Dordrecht, Springer.
36 Nagajyoti PC, Lee KD, Sreekanth TVM. 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8: 199-216.   DOI
37 Thornton I, Rautiu R, Brush S. 2001. Lead: The Facts. Ian Allan Printing Ltd., London.
38 Triantafyllidou S, Edwards M. 2009. Lead (Pb) in U.S. drinking water: school case studies, detection challenges and public health considerations. In: Your Drinking Water: Challenges and Solutions for the 21st Century. Drinking Water Symposium, April 20th & 21st, 2009, Yale University.
39 Dermont G, Bergeron M, Mercier G, Richer-Lafleche M. 2008. Soil washing for metal removal: a review of physical/ chemical technologies and field applications. J. Hazard. Mater. 152: 1-31.   DOI
40 Jabeen R, Ahmad A, Iqbal M. 2009. Phytoremediation of heavy metals: physiological and molecular mechanisms. Bot. Rev. 75: 339-364.   DOI
41 Jiang CY, Sheng XF, Qian M, Wang QY. 2008. Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72: 157-164.   DOI
42 Sheng XF, Jiang CY, He LY. 2008. Characterization of plant growth-promoting Bacillus edaphicus NBT and its effect on lead uptake by Indian mustard in a lead-amended soil. Can. J. Microbiol. 54: 417-422.   DOI
43 Sheng XF, Xia JJ. 2006. Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64: 1036-1042.   DOI
44 Sheng X-F, Xia JJ, Jiang CY, He LY, Qian M. 2008. Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ. Pollut. 156: 1164-1170.   DOI
45 Usman ARA, Almaroai YA, Ahmad M, Vithanage M, Ok YS. 2013. Toxicity of synthetic chelators and metal availability in poultry manure amended Cd, Pb and As contaminated agricultural soil. J. Hazard. Mater. 262: 1022-1030.   DOI
46 Lindsay WL. 1979. Chemical Equilibrium in Soils. Wiley Interscience Publishers, New York.
47 Zhao S, Jia L, Duo L. 2013. The use of biodegradable chelators for enhanced phytoextraction of heavy metals by Festuca arundinacea from municipal solid waste compost and associated heavy metal leaching. Bioresour. Technol. 129: 249-255.   DOI
48 Evangelou MWH, Bauer U, Ebel M, Schaeffer A. 2007. The influence of EDDS and EDTA on the uptake of heavy metals of Cd and Cu from soil with tobacco, Nicotiana tabacum. Chemosphere 68: 345-353.   DOI
49 Fasim F, Ahmed N, Parsons R, Gadd GM. 2002. Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery. FEMS Microbiol. Lett. 213: 1-6.   DOI
50 Long XX, Chen XM, Chen YG, Wong JW-C, Wei ZB, Wu QT. 2011. Isolation and characterization endophytic bacteria from hyperaccumulator Sedum alfredii Hance and their potential to promote phytoextraction of zinc polluted soil. World J. Microbiol. Biotechnol. 27: 1197-1207.   DOI
51 Braud A, Jezequel K, Vieille E, Tritter A, Lebeau T. 2006. Changes in extractability of Cr and Pb in a poly contaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Water Air Soil Pollut. 6: 261-279.   DOI
52 Zheljazkov VD, Nielsen NE. 1996. Effect of heavy metals on peppermint and cornmint. Plant Soil 178: 59-66.   DOI
53 Nelson DW, Sommers LE. 1996. Total carbon, organic carbon, and organic matter, pp. 961-1010. In Sparks DL (ed.), Method of Soil Analysis, Part 3, Chemical Methods. Soil Science Society of America, Inc., American Society of Agronomy, Madison, WI.