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Copper-tolerant rhizosphere bacteria—characterization and assessment of plant growth promoting factors

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Abstract

Remediation of heavy metal contaminated soil is a major problem or concern worldwide. Heavy metal accumulation in the soil is increasing day by day by industries, mines, agriculture, fuel combustion and municipal waste discharge. Such contaminated soils harbour a large number of resistant microbial populations. Screening and isolation of such microbes would be utilized for natural remediation of metal contaminated soils. Therefore, in the present study, highly copper-tolerant bacteria from rhizosphere soil of Cynodon dactylon grown in brass effluent contaminated soil were isolated and assessed for plant growth promoting factors. A total of 61 isolates were isolated from the rhizosphere of three contaminated sites. Six highly copper-tolerant isolates named as MYS1, MYS2, MYS3, MYS4, MYS5 and MYS6 were isolated through enrichment in copper containing nutrient broth. 16S rRNA analysis revealed that the isolates were from genera Stenotrophomonas and Brevundimonas and belong to classes Alpha Proteobacteriacea and Gamma Proteobacteriacea, respectively. Strain MYS1, MYS2 and MYS4 showed 95–99% similarity with Stenotrophomonas acidaminiphila, strain MYS3 and MYS5 showed 99 and 97% similarity with Stenotrophomonas maltophilia and Stenotrophomonas sp. Strain MYS6 showed 94% similarity with Brevundimonas diminuta. All the rhizobacteria showed plant growth promoting traits such as production of siderophores, indole acetic acid (IAA), phosphate solubilization and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity. From this study, we can conclude that all the isolates possess copper resistance and potential for phytoremediation of copper polluted soils.

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References

  • Aksorn E, Chitsomboon B (2013) The effects of plant growth promoting traits on heavy metal uptake of Vetiver grasss. Am-Eur J Agric Environ Sci 13:465–470

    CAS  Google Scholar 

  • Altimira F, Yáñez C, Bravo G, González MA, Rojas L, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:193

    Article  CAS  Google Scholar 

  • Andreazza R, Okeke BC, Lambais MR, Bortolon L, Bastos de Melo GW, Camargo FAO (2010) Bacterial stimulation of copper phytoaccumulation by bioaugmentation with rhizosphere bacteria. Chemosphere 81:1149–1154

    Article  CAS  Google Scholar 

  • Atlas RM, Bartha R (1998) Fundamentals and applications. In: microbial ecology, 4th edn. Benjamin/Cummings Publishing Company, Inc., California, USA, pp 523–530

    Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth promoting rhizobacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.) Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Berg J, Brandt KK, Al-Soud WA, Holm PE, Hansen LH, Sørensen SJ, Nybroe O (2012) Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Appl Environ Microbiol 78:7438–7446

    Article  CAS  Google Scholar 

  • Bhattacharya A (2010) Siderophore mediated metal uptake by Pseudomonas fluorescens and its comparison to iron (iii) chelation. Ceylon J Sci 39:147–155

    Google Scholar 

  • Bolan NS, Naidu R, Mahimairaja S, Baskaran S (1994) Influence of low-molecular-weight organic acids on the solubilisation of phosphates. Biol Fert Soils 18:311–319

    Article  CAS  Google Scholar 

  • Bremner J (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33

    Article  CAS  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668

    CAS  Google Scholar 

  • Cavalca L, Zanchi R, Corsini A, Colombo M, Romagnoli C, Canzi E, Andreoni V (2010) Arsenic-resistant bacteria associated with roots of the wild Cirsium arvense (L.) plant from an arsenic polluted soil, and screening of potential plant growth-promoting characteristics. Syst Appl Microbiol 33:154–164

    Article  CAS  Google Scholar 

  • Cervantes C, Gutierrez-Corona F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137

    Article  CAS  Google Scholar 

  • Chehregani A, Malayeri BE (2007) Removal of heavy metals by native accumulator plants. Int J Agric Biol 9:462–465

    CAS  Google Scholar 

  • Dell'Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84

    Article  Google Scholar 

  • Dhiman SS, Selvaraj C, Li J, Singh R, Zhao X, Kim D, Kim JY, Kang YC, Lee JK (2016) Phytoremediation of metal-contaminated soils by the hyperaccumulator canola (Brassica napus L.) and the use of its biomass for ethanol production. Fuel 183:107–114

    Article  CAS  Google Scholar 

  • Dworkin M, Foster JW (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–603

    CAS  Google Scholar 

  • Farkas E, Csóka H, Micera G, Dessi A (1997) Copper (II), nickel (II), zinc (II), and molybdenum (VI) complexes of desferrioxamine B in aqueous solution. J Inorg Biochem 65:281–286

    Article  CAS  Google Scholar 

  • Fässler E, Evangelou MW, Robinson BH, Schulin R (2010) Effects of indole-3-acetic acid (IAA) on sunflower growth and heavy metal uptake in combination with ethylene diamine disuccinic acid (EDDS). Chemosphere 80:901–907

    Article  Google Scholar 

  • Feris K, Ramsey P, Frazar C, Moore JN, Gannon JE, Holbert WE (2003) Differences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Appl Environ Microbiol 69:5563–5573

    Article  CAS  Google Scholar 

  • Gang A, Vyas A, Vyas H (2013) Toxic effect of heavy metals on germination and seedling growth of wheat. J Environ Res Dev 8:206–213

    CAS  Google Scholar 

  • Ghosh A, Saha PD (2013) Optimization of copper bioremediation by Stenotrophomonas maltophilia PD2. J Environ Chem Eng 1:159–163

    Article  CAS  Google Scholar 

  • Ghosh P, Rathinasabapathi B, Ma LQ (2011) Arsenic-resistant bacteria solubilized arsenic in the growth media and increased growth of arsenic hyperaccumulator Pteris vittata L. Bioresour Technol 102:8756–8761

    Article  CAS  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68

    Article  CAS  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    Article  CAS  Google Scholar 

  • Gordon AS, Howell LD, Harwood V (1994) Responses of diverse heterotrophic bacteria to elevated copper concentrations. Can J Microbiol 40:408–411

    Article  CAS  Google Scholar 

  • Gupta R, Rekha S, Aparna S, Kuhad RC (1994) A modified plate assay for screening phosphate solubilizing microorganisms. J Gen Appl Microbiol 40:255–260

    Article  CAS  Google Scholar 

  • Huang X, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2004) A multi-process phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environ Pollut 130:465–476

    Article  CAS  Google Scholar 

  • Iyaka YA, Kakulu SE (2012) Topsoil contamination by heavy metals from a local brass industrial area of Nigeria. Resour Environ 2:86–89

    Article  Google Scholar 

  • Jang CS, Liu CW, Lin KH, Wang SW (2006) Spatial analysis of potential carcinogenic risk associated with ingesting arsenic in aquaculture tilapia (Oreochromis mossambicus) in black foot disease hyper endemic area. Environ Sci Technol 40:1707–1717

    Article  CAS  Google Scholar 

  • Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–474

    Article  CAS  Google Scholar 

  • Kim BK, De Macario EC, Nolling J, Daniels L (1996) Isolation and characterization of copper resistant methanogens from a copper mining soil sample. Appl Environ Microbiol 62:2629–2635

    CAS  Google Scholar 

  • Kozdroj J (1995) Microbial response to single or successive soil contamination with Cd2+ or Cu2+. Soil Biol Biochem 27:1459–1465

    Article  CAS  Google Scholar 

  • Li J, Xie ZM, Xu JM, Sun YF (2006) Risk assessment for safety of soils and vegetables around a lead/zinc mine. Environ Geochem Health 28:37–44

    Article  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Improvement of plant growth and nickel uptake by nickel resistant-plant growth promoting bacteria. J Hazard Mater 166:1154–1161

    Article  CAS  Google Scholar 

  • Ma Y, Oliveria RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69

    Article  CAS  Google Scholar 

  • Mathur N, Kumar A (2013) Physico-chemical characterization of industrial effluents contaminated soil of Sanganer. J Emerging Trends Eng and Appl Sci 4:226–228

    CAS  Google Scholar 

  • Michels HT (2006) Anti-microbial characteristics of copper. ASTM Standardization News:28–31

  • Mujahid TY, Siddiqui K, Ahmed R, Kazmi SU, Ahmed N (2014) Isolation and partial characterization of phosphate solubilising bacteria isolated from soil and marine samples. Pak J Pharm Sci 27:1483–1490

    Google Scholar 

  • Mumoz M, Pena L, Halloroms JO (1994) Use of an industrial by product as a liming source. J Agric Univ P R 78:195–202

    Google Scholar 

  • Okalebo JR, Gathua KW, Woomer PL (1993) Laboratory methods of soil and plant analysis: a working manual tropical soil biology and fertility program. TSBF Institute, Nairobi, Kenya

    Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Washington, USDA

    Google Scholar 

  • Opulencia RB, Bambase ME, Perdigon KMD, Demafelis RB, Llamado AA, Franco RAG, Mogul RT, Raymundo AK (2015) Copper-resistant, biofilm-forming bacteria for potential use in rehabilitation of copper-contaminated wastewater. Int J Phil Sci Technol 8:56–60

    Article  Google Scholar 

  • Oviasogie PO, Omoruyi E (2007) Levels of heavy metals and physicochemical properties of soil in a foam manufacturing industry. J Chem Soc Niger 32:102–106

    CAS  Google Scholar 

  • Partha V, Murthya NN, Saxen PR (2011) Assessment of heavy metal contamination in soil around hazardous waste disposal sites in Hyderabad city (India): natural and anthropogenic implications. J Environ Res Manage 2:27–34

    Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiologiya 17:362–370

    CAS  Google Scholar 

  • Płociniczaka T, Sinkkonenb A, Romantschukb M, Piotrowska-Sege Z (2013) Characterization of Enterobacter intermedius MH8b and its use for the enhancement of heavy metals uptake by Sinapis alba L. Appl Soil Ecol 63:1–7

    Article  Google Scholar 

  • Premono M, Moawad MA, Vleck PLG (1996) Effect of phosphate solubilizing Pseudmonas putida on the growth of maize and its survival in the rhizosphere. Indonesian J Crop Sci 11:13–23

    Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149

  • Rathaur P, Ramteke PW, Raja W, John SA (2012) Isolation and characterization of nickel and cadmium tolerant plant growth promoting rhizobacteria from rhizosphere of Withania somnifera. J Biodiver Environ Sci 6:253–261

    Google Scholar 

  • Sabry M, Shaheen CD, Tsadilas T (2009) Distribution coefficient of copper in different soils from Egypt and Greece. Commun Soil Sci Plant 40:214–226

    Article  Google Scholar 

  • Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Chemosphere 160:47–56

    CAS  Google Scholar 

  • SEEPA (1995) Environmental quality standards for soils. State Environmental Protection Administration, China GB15618

    Google Scholar 

  • Shakoori AR, Muneer B (2001) Copper-resistant bacteria from industrial effluents and their role in remediation of heavy metals in wastewater. Folia Microbiol 47:43–50

    Article  Google Scholar 

  • Sharma RS, Mohmmed A, Mishra V, Babu CR (2005) Diversity in promiscuous group of rhizobia from three Sesbania spp. colonizing ecologically distinct habitats of the semi-arid Delhi region. Res Microbiol 156:57–67

    Article  CAS  Google Scholar 

  • Sharma RS, Mishra V, Mohmmed A, Babu CR (2008) Phage specificity and lipopolysaccharides of stem and root-nodulating bacteria (Azorhizobium caulinodans, Sinorhizobium spp., and Rhizobium spp.) of Sesbania spp. Arch Microbiol 189:411–418

    Article  CAS  Google Scholar 

  • Singh Y, Ramteke PW, Shukla PK (2013) Isolation and characterization of heavy metal resistant Pseudomonas spp. and their plant growth promoting activities. Adv Appl Sci Res 4:269–272

    CAS  Google Scholar 

  • Singh V, Ram C, Kumar A (2016) Physico-chemical characterization of electroplating industrial effluents of Chandigarh and Haryana region. J Civil Environ Eng 6:237. doi:10.4172/2165-784X.1000237

    Article  Google Scholar 

  • Song J, Zhao FJ, Luo YM, McGrath SP, Zhang H (2004) Copper uptake by Elsholtzia splendens and Silene vulgaris and assessment of copper phytoavailability in contaminated soils. Environ Pollut 128:307–315

    Article  CAS  Google Scholar 

  • Ssenku JE, Ntale M, Origa HO (2014) Physico-chemical characteristics of copper tailings and pyrite soils in western Uganda: implication for phytoremediation. Int J Environ Monit Anal 2:191–198

    Article  CAS  Google Scholar 

  • Walkley A, Black IA (1934) An examination of the degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    Article  CAS  Google Scholar 

  • WHO (2010) Guideline for drinking water quality recommendations, (Vol. 1). World Health Organization, Geneva

    Google Scholar 

  • Xiao J, Guo L, Wang S, Lu Y (2010) Comparative impact of cadmium on two phenanthrene-degrading bacteria isolated from cadmium and phenanthrene co-contaminated soil in China. J Hazard Mater 174:818–823

    Article  CAS  Google Scholar 

  • Xu J, Yang L, Wang Z, Dong G, Huang J, Wang Y (2006) Toxicity of copper on rice growth and accumulation of copper in rice grain in copper contaminated soil. Chemosphere 62:602–607

    Article  CAS  Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997

    Article  CAS  Google Scholar 

  • Zaki S, Farag S (2010) Isolation and molecular characterization of some copper biosorped strains. Int J Environ Sci Technol 7:553–560

    Article  CAS  Google Scholar 

  • Zhang YF, He LY, Chen ZJ, Wang QY, Qian M, Sheng XF (2011) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 83:57–62

    Article  CAS  Google Scholar 

  • Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth promoting rhizobacteria for bioremediation. Environ Int 3:406–413

    Article  Google Scholar 

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Acknowledgements

The authors wish to acknowledge the Department of Science and Technology and Sophisticated Analytical Instrument Facility of IIT Madras for their support in metal analysis.

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Correspondence to Yogalakshmi Kadapakkam Nandabalan.

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Rathi, M., Nandabalan, Y.K. Copper-tolerant rhizosphere bacteria—characterization and assessment of plant growth promoting factors. Environ Sci Pollut Res 24, 9723–9733 (2017). https://doi.org/10.1007/s11356-017-8624-2

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