Abstract
The heavy metals at high concentration are generally toxic to the plants for their metabolism and growth; therefore, interactions among metals, rhizosphere microbes and plants have attracted attention because of the biotechnological potential of microorganisms for metal removal directly from contaminated soils or the possible transference of them to the plants. The aim of this study was to compare the relationships between the physiological in vitro characteristics of rhizobacteria isolated from plant metal accumulators and their distribution relating with the heavy metals content in contaminated soils. The results of this study showed that the heavy metals present in the rhizosphere of the plant species analyzed, decrease the microbial biomass and content of heavy metals caused a different distribution of rhizobacteria found. Gram negative rhizobacteria (90 %) and gram positive rhizobacteria (10 %) were isolated; all of them are metal-resistant rhizobacteria and 50 % of the isolated rhizobacteria possess both traits: higher indol acetic acid and siderophore producers. The inoculation with these rhizosphere microorganisms that possess metal-tolerating ability and plant growth promoting activities, can be recommended with a practical importance for both metal-contaminated environment and plant growth promotion.
Similar content being viewed by others
References
Abaye, D. A.; Lawlor, K.; Hirsch, P. R.; Brookes, P. C., (2005). Changes in the microbial community of an arable soil caused by long-term metal contamination. Eur. J. Soil Sci., 56(1), 93–102 (10 pages).
Abou-Shanab, R. A.; Angle, J. S.; Delorme, T. A.; Chaney, R. L.; van Berkum, P.; Moawad, H.; Ghanem, K.; Ghozlan, H. A., (2003). Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale, New Phytol., 158(1), 219–224 (6 pages).
Aceves, J., (2003). GraphPad Software. GraphPad InStat, V2.03
Ahmad, F.; Ahmad, I.; Khan, M. S., (2005). Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk. J. Biol., 29(1), 29–34 (6 pages).
Ahmad, F.; Ahmad, I.; Khan, M. S., (2008). Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol. Res., 163(2), 173–181 (9 pages).
Allers, T.; Lichen, M., (2000). A method for preparing genomic DNA that restrains branch migration of Holiday junctions. Nucl. Aci. Res., 28(2), 26–36 (11 pages).
Barazani, O. Z.; Friedman, J., (1999). Is IAA the major root growth factor secreted from plant-growth-mediating bacteria. J. Chem. Ecol., 25(10), 2397–2406 (10 pages).
Belimov, A. A.; Hontzeas, N.; Safronova, V. I.; Demchinskaya, S. V.; Piluzza, G.; Bullitta, S.; Glick, B. R., (2005). Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea LCzern.). Soil Biol. Biochem., 37(2), 241–250 (10 pages).
Black, R. C.; Choate, D. M.; Bardhan, S.; Revis, N.; Barton, L. L.; Zocco, T. G., (1993). Chemical transformation of toxic metals by a Pseudomonas strain from a toxic waste site. Environ. Toxicol. Chem., 12(8), 1365–1376 (12 pages).
Bremer, P.J.; Geasey, G.G., (1993). Interactions of bacteria with metals in the aquatic environment. in: Rao, S.S. (Ed.), Particulate Matter and Aquatic Contaminants. Lewis Publishers, Boca Raton.
Bric, J. M.; Bostock, R. M.; Silversone, S. E., (1991). Rapid in situ assay for indole acetic acid production by bacteria immobilization on a nitrocellulose membrane. Appl. Environ. Microbiol., 57(2), 535–538 (4 pages).
Burd, G. I.; Dixon, D. G.; Glick. B. R., (1998). A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol., 64(10), 3663–3668 (6 pages).
Burd G. I.; Dixon, D. G.; Glick. B. R., (2000). Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can. J. Microbiol., 46(3), 237–245 (9 pages).
Churchill, S. A.; Walters, J. V.; Churchill, P. F., (1995). Sorption of heavy metals by prepared bacterial cell surfaces. J. Environ. Eng., 121(10), 706–711 (6 pages).
Clarke, S. E.; Stuart, J.; Sandersloehr, J., (1987). Induction of siderophore activity in Anabaena species and its moderation of copper toxicity. Appl. Environ. Microbiol., 53(5), 917–922 (6 pages).
Dell’ Amico, H.; Cavalca, L.; Andreoni, V., (2005). Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS. Microbiol. Ecol., 52(2), 153–162 (10 pages).
Dell’Amico, H.; Cavalca, L.; Andreoni, V., (2008). Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol. Biochem., 40(1), 74–84 (11 pages).
De Souza, M. P.; Huang, C. P. A.; Chee, N.; Terry, N., (1999). Rhizosphere bacteria enhance that accumulation of selenium and mercury in wetland plants. Planta, 209(2), 259–263 (5 pages).
Egamberdiyeva, D.; Hoflich, G., (2004). Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J. Arid Environ., 56(2), 293–301 (9 pages).
Epelde L.; Becerril, J. M.; Barrutia, O.; González-Oreja, J. A.; Garbisu, C., (2010). Interactions between plant and rhizosphere microbial communities in a metalliferous soil. Environ. Poll., 158(5), 1576–1583 (8 pages).
Erbe, J. L.; Taylor, K. B.; Hall, L. M., (1995). Metalloregulation of the cyanobacterial smt locus: identification of the smtB binding sites and direct interaction with metals. Nucl. Acid Res., 23(13), 2472–2478 (7 pages).
Franco-Hernández, M. O.; Vásquez-Murrieta, M. S.; Patiño-Siciliano, A.; Dendooven, L., (2010). Heavy metals concentration in plants growing on mine tailings in Central Mexico. Bioresour. Tech., 101(11), 3864–3869 (6 pages).
Frostegård, A.; Tunlid, A.; Bååth, E., (1993). Phospholipid fatty acid composition, biomass and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl. Environ. Microbiol., 59(11), 3605–3617 (13 pages).
Gadd, G. M., (1990). Heavy metal accumulation by bacteria and other microorganisms. Experientia, 46(8), 834–840 (7 pages).
Glick, B. R.; Penrose, D. M.; Li, J., (1998). A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J. Theor. Biol., 190(1), 63–68 (6 pages).
Glick, B. R., (2003). Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotech. Adv., 21(5), 383–393 (11 pages).
Guo, L.; Andrews, J.; Riding, R.; Dennis, P.; Dresser, Q., (1996). Possible microbial effects on stable carbon isotopes in hot-spring travertines. J. Sediment. Res., 66(3), 468–473 (6 pages).
Idris, R.; Trifonova, M.; Puschenreiter, W.; Wenzel, W.; Sessitsch, A., (2004). Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl. Environ. Microbiol., 70(5), 2667–2677 (11 pages).
Khalid, A.; Arshad, M.; Zahir, Z. A., (2004). Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol., 96(3), 473–480 (8 pages).
Khan, A. G., (2005). Role of soil microbes in the rhizosphere of plants growing on trace metal contaminated soils in phytoremediation. J. Trace Elem. Med. Biol., 18(4), 355–364 (10 pages).
Li, J.; Zu, J.; Tang, C.; Wu, J.; Muhammad, A.; Wang, H., (2005). Application of 16S rDNA PCR amplification and DDGE fingerprinting for detection of shift in microbial community diversity in Cu, Zn and Cd contaminated paddy soils. Chemosphere, 62(8), 1375–1380 (6 pages).
Ma, Y.; Rajkumar, M.; Freitas, H., (2009). Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J. Hazard. Mater., 166(2–3), 1154–1161 (8 pages).
Mantelin, S.; Touraine, B., (2004). Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J. Exp. Bot., 55(394), 27–34 (8 pages).
Nouri, J.; Lorestani, B.; Yousefi, N.; Khorasani, N.; Hasani, A. H.; Seif, S.; Cheraghi, M., (2011). Phytoremediation potential of native plants grown in the vicinity of Ahangaran lead-zinc mine (Hamedan, Iran). Environ. Earth Sci., 62(3), 639–644 (6 pages).
Piotrowska-Seget, Z.; Cycon, M.; Kozdroj, J., (2005). Metal-tolerant bacteria occurring in heavily polluted soil and mine spoil. Appl. Soil Ecol., 28(3), 237–246 (10 pages).
Ramsey, P. W.; Rillig, M. C.; Feris, K. P.; Gordon, N. S.; Moore, J. N.; Holben, W. E.; Gannon, J. E., (2005). Relationship between communities and processes; newinsights froma field study of a contaminated ecosystem. Ecol. Lett., 8(11), 1201–1210 (10 pages).
Rau, N.; Mishra, V.; Sharma, M.; Das, M.; Ahaluwalia, K.; Sharma, R. S., (2009). Evaluation of functional diversity in rhizobacterial taxa of a wild grass (Saccharum ravennae) colonizing abandoned fly ash dumps in Delhi urban ecosystem. Soil. Biol. Biochem., 41(4), 813–821 (9 pages).
Rohlf, J., (2004). NTSYS-PC Version 2.11T. Numerical Taxonomy and Multivariate Analysis System. Applied Bioestastistics, Inc.
Schwyn, B.; Neilands, J. B., (1987). Universal chemical assay for the detection and determination of siderophores. Analys. Biochem., 160(1), 47–56 (10 pages).
Sharma, M.; Rau, N.; Mishra, V.; Sharma, R. S., (2005). Unexplored ecological significance of Saccharum munja. Species, 43, 22 (1 pages).
Phage specificity and lipopolysaccharides of stem- and root-nodulating bacteria (Azorhizobium caulinodans, Sinorhizobium spp., and Rhizobium spp.) of Sesbania spp. Arch. Microbiol., 189(4), 411–418 (8 pages).
Sheng, X. F.; Xia, J. J., (2006). Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere, 64(6), 1036–1042 (7 pages).
Sheng, F. X.; Xia, J. J.; Jiang, Ch.Y.; He, L. Y.; 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. Poll., 156(3), 1164–1170 (7 pages).
Sneath, P. H. A.; Sokal, R. R., (1973). Numerical Taxonomy: the principles and practice of numerical classification. Freeman, San Francisco.
Vásquez-Murrieta, M. S.; Migueles-Garduño, I.; Franco-Hernández, O.; Govaerts, B.; Dendooven, L., (2006). C and N mineralization and microbial biomass in heavy metal-contaminated soil. Eur. J. Soil, Biol., 42(2), 89–98 (10 pages).
Wardle, D. A.; Bonner, K. I.; Barker, G. M.; Yeates, G. W.; Nicholson, K. S.; Bardgett, R. D.; Watson, R. N.; Ghani, A., (1999). Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol. Monogr., 69(4), 535–568 (33 pages).
Weisburg, W. G.; Barns, S. M.; Pelletier, D. A.; Lane, D. J., (1991). 16Ribosomal DNA amplification for phylogenetic study. J. Bacteriol., 173(2), 697–703 (7 pages).
Wenzel, W. W.; Lombi, E.; Adriano, D. C., (1999). Biogeochemical processes in the rhizosphere: role in phytoremediation of metal-polluted sites. in: Prasad, M.N.V., Hagemeyer, J. (Eds.), Heavy Metal Stress in Plants: from Molecules to Ecosystems. Springer, Heidelberg, Berlin, New Yo
Whiting, S. N.; De Souza, M. P.; Terry, N., (2001). Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ. Sci. Tech., 35(15), 3144–3150 (7 pages).
Wong, M. H., (2003). Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere, 50(6), 775–780 (6 pages).
Wu, S. C.; Cao, Z. H.; Li, Z. G.; Cheung, K. C.; 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(1–2), 155–166 (12 pages).
Wu S.C.; Peng, X. L.; Cheung, K. C.; Liu, S. L.; Wong, M. H., (2009). Adsorption kinetics of Pb and Cd by two plant growth promoting rhizobacteria. Bioresour. Tech., 100(20), 4559–4563 (5 pages).
Young, K. D., (2006). The selective value of bacterial shape. Microbiol. Mol. Biol. R., 70(3), 660–703 (44 pages).
Zaidi, S.; Usmami, S.; Singh, B. R.; Musarrat, J., (2006). Significancce of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant grown promotion and nickel accumulation in Brassica juncea. Chemosphere, 64(6), 991–997 (7 pages).
Zhuang, X.; Chen, J.; Shim, H.; Bai, Z., (2007). New advances in plant growth promoting rhizobacteria for bioremediation. Environ. Int., 33(3), 406–413 (8 pages).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Melo, M.R., Flores, N.R., Murrieta, S.V. et al. Comparative plant growth promoting traits and distribution of rhizobacteria associated with heavy metals in contaminated soils. Int. J. Environ. Sci. Technol. 8, 807–816 (2011). https://doi.org/10.1007/BF03326264
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF03326264