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Genetic and biochemical characterization of rhizobacterial strains and their potential use in combination with chelants for assisted phytoremediation

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An Erratum to this article was published on 24 February 2017

Abstract

Copper and zinc are essential micronutrients in plants but, at high concentrations, they are toxic. Assisted phytoremediation is an emerging “green” technology that aims to improve the efficiency of tolerant species to remove metals from soils through the use of chelants or microorganisms. Rhizobacteria can promote plant growth and tolerance and also affect the mobility, bioavailability, and complexation of metals. A pot experiment was conducted to evaluate the phytoremediation effectiveness of sunflowers cultivated in a Cu- and Zn-spiked soil, in the presence or absence of bacterial consortium and/or chelants. The consortium was constituted of two Stenotrophomonas maltophilia strains and one of Agrobacterium sp. These strains were previously isolated from the rhizosphere of maize plants cultivated on a metal-polluted soil and here molecularly and biochemically characterized. Results showed that the consortium improved sunflower growth and biomass production on the spiked soils. Sunflowers accumulated large amounts of metals in their roots and leaves; however, neither the bacterial consortium nor the chelants, singularly added to pots, influenced significantly Cu and Zn plant uptake. Furthermore, the consecutive soil amendment with the EDTA and bacterial consortium determined a consistent accumulation of metals in sunflowers, and it might be an alternative strategy to limit the use of EDTA and its associated environmental risks in phytoremediation.

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References

  • Ahemad M (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. Biotech 5:111–121

    Google Scholar 

  • Ali H, Khan E, Anwar SM (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881

    Article  CAS  Google Scholar 

  • Baldantoni D, Ligrone R, Alfani A (2009) Macro- and trace-element concentrations in leaves and roots of Phragmites australis in a volcanic lake in Southern Italy. J Geochem Explor 101:166–174

    Article  CAS  Google Scholar 

  • Baldantoni D, Cicatelli A, Castiglione S (2011) Genetic biodiversity of maize and sunflower commercial cultivars, and their phytoextraction capability of a multi-metal artificially polluted soil. In: Golubev IA (ed) Handbook of phytoremediation, Nova Science Publishers, Inc. New York-US, pp 631–649.:

  • Baldantoni D, Cicatelli A, Bellino A, Castiglione S (2014) Different behaviours in phytoremediation capacity of two heavy metal tolerant poplar clones in relation to iron and other trace elements. J Environ Manag 146:94–99

    Article  CAS  Google Scholar 

  • Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T et al (2014) Remediation of heavy metal(loid)s contaminated soils—to mobilize or to immobilize? J Hazard Mater 266:141–166

    Article  CAS  Google Scholar 

  • Boltz DF, Howell JA (1978) Colorimetric determination of nonmetals. John Wiley & Sons, New York

    Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    Article  CAS  Google Scholar 

  • Chaney RL (1983) Plant uptake of inorganic waste constituents. In: Parr JFEA (ed) Land treatment of hazardous wastes. Noyes Data Corp, New Jork, pp. 50–76

    Google Scholar 

  • Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302

    Article  Google Scholar 

  • Evangelou MW, 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

    Article  CAS  Google Scholar 

  • Faessler E, Robinson BH, Stauffer W, Gupta SK, Papritz A, Schulin R (2010) Phytomanagement of metal-contaminated agricultural land using sunflower, maize and tobacco. Agric Ecosyst Environ 136:49–58

    Article  CAS  Google Scholar 

  • Gamalero E, Glick BR (2015) Bacterial modulation of plant ethylene levels. Plant Physiol 169:13–22

    Article  CAS  Google Scholar 

  • Gheju M, Stelescu I (2013) Chelant-assisted phytoextraction and accumulation of Zn by Zea mays. J Environ Manag 128:631–636

    Article  CAS  Google Scholar 

  • Glick BR, Penrose DM, Li JP (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 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374

    Article  CAS  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  Google Scholar 

  • Goldstein AH (1986) Bacterial solubilization of mineral phosphates: historical perspectives and future prospects. Am J Altern Agric 1:51–57

    Article  Google Scholar 

  • Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda C, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3. Biotech 5:355–377

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977

    Article  CAS  Google Scholar 

  • He LY, Zhang YF, Ma HY, Su LN, Chen ZJ, Wang QY et al (2010) Characterization of copper-resistant bacteria and assessment of bacterial communities in rhizosphere soils of copper-tolerant plants. Appl Soil Ecol 44:49–55

    Article  Google Scholar 

  • Holmes A, Vinayak A, Benton C, Esbenshade A, Heinselman C, Frankland D et al (2009) Comparison of two multimetal resistant bacterial strains: Enterobacter sp YSU and Stenotrophomonas maltophilia ORO2. Curr Microbiol 59:526–531

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kabata-Pendias A, (2011) Trace elements in soils and plants, 4th edn. Taylor and Francis Group London.

  • Kirchhof G, Reis VM, Baldani JI, Eckert B, Dobereiner J, Hartmann A (1997) Occurrence, physiological and molecular analysis of endophytic diazotrophic bacteria in gramineous energy plants. Plant Soil 194:45–55

    Article  CAS  Google Scholar 

  • Kolbas A, Kidd P, Guinberteau J, Jaunatre R, Herzig R, Mench M (2015) Endophytic bacteria take the challenge to improve Cu phytoextraction by sunflower. Environ Sci Pollut R 22:5370–5382

    Article  CAS  Google Scholar 

  • Langella F, Grawunder A, Stark R, Weist A, Merten D, Haferburg G et al (2014) Microbially assisted phytoremediation approaches for two multi-element contaminated sites. Environ Sci Pollut R 21:6845–6858

    Article  CAS  Google Scholar 

  • Lin JJ, Kuo J, Ma J (1996) A PCR-based DNA fingerprinting technique: AFLP for molecular typing of bacteria. Nucleic Acids Res 24:3649–3650

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lingua G, Todeschini V, Grimaldi M, Baldantoni D, Proto A, Cicatelli A et al (2014) Polyaspartate, a biodegradable chelant that improves the phytoremediation potential of poplar in a highly metal-contaminated agricultural soil. J Environ Manag 132:9–15

    Article  CAS  Google Scholar 

  • Liu ST, Kado CI (1979) Indoleacetic acid production: a plasmid function of Agrobacterium tumefaciens C58. Biochem Bioph Res Co 90:171–178

    Article  CAS  Google Scholar 

  • Looney W, Narita M, Muehlemann K (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9:312–323

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25

    Article  CAS  Google Scholar 

  • Madejon P, Murillo JM, Maranon T, Cabrera F, Soriano MA (2003) Trace element and nutrient accumulation in sunflower plants two years after the Aznalcollar mine spill. Sci Total Environ 307:239–257

    Article  CAS  Google Scholar 

  • Meers E, Ruttens A, Hopgood MJ, Samson D, Tack FMG (2005) Comparison of EDTA and EDDS as potential soil amendments for enhanced phytoextraction of heavy metals. Chemosphere 58:1011–1022

    Article  CAS  Google Scholar 

  • Mehlich A (1938) Use of triethanolamine acetate-barium hydroxide buffer for the determination of some base exchange properties and lime requirement of soil. Soil Sci SocAmProc 29:374–378

    Google Scholar 

  • Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775

    Article  CAS  Google Scholar 

  • Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotech Adv 32:429–448

    Article  Google Scholar 

  • Nehnevajova E, Lyubenova L, Herzig R, Schroeder P, Schwitzguebel JP, Schmuelling T (2012) Metal accumulation and response of antioxidant enzymes in seedlings and adult sunflower mutants with improved metal removal traits on a metal-contaminated soil. Environ Exp Bot 76:39–48

    Article  CAS  Google Scholar 

  • Neilands JB (1995) Siderophores—structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726

    Article  CAS  Google Scholar 

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

  • Ortiz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712

    Article  CAS  Google Scholar 

  • Patten CL, Glick BR (2002) Regulation of indoleacetic acid production in Pseudomonas putida GR12-2 by tryptophan and the stationary-phase sigma factor RpoS. Can JMicrobiol 48:635–642

    Article  CAS  Google Scholar 

  • Piotrowska-Seget Z, Cycon M, Kozdroj J (2005) Metal-tolerant bacteria occurring in heavily polluted soil and mine spoil. Appl Soil Ecol 28:237–246

    Article  Google Scholar 

  • Prapagdee B, Chanprasert M, Mongkolsuk S (2013) Bioaugmentation with cadmium-resistant plant growth-promoting rhizobacteria to assist cadmium phytoextraction by Helianthus annuus. Chemosphere 92:659–666

    Article  CAS  Google Scholar 

  • Rademaker JLW, Hoste B, Louws FJ, Kersters K, Swings J, Vauterin L, Vauterin P, de Bruijn FJ (2000) Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system. International Journal Of Systematic and Evolutionary Microbiology 50: 655–677. Rahman MM, Azirun SM, Boyce AN (2013) Enhanced accumulation of copper and lead in amaranth (Amaranthus paniculatus), Indian mustard (Brassica juncea) and sunflower (Helianthus annuus). Plos One 8.

  • Rajkumar M, Sandhya S, Prasad M, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechn Adv 30:1562–1574

    Article  CAS  Google Scholar 

  • Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB et al (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shahid M, Austruy A, Echevarria G, Arshad M, Sanaullah M, Aslam M et al (2014) EDTA-enhanced phytoremediation of heavy metals: a review. Soil & Sediment Contamination 23:389–416

    Article  CAS  Google Scholar 

  • Tak HI, Ahmad F, Babalola OO (2013) Advances in the application of plant growth-promoting rhizobacteria in phytoremediation of heavy metals. Whitacre (ed) Reviews of environmental contamination and toxicology 223:33–52

    CAS  Google Scholar 

  • Thomas JW, Branden YA, Howard RD (2004) NIST standard reference materials catalog 2004. Special Publication (NIST SP) - 260

  • Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21-3:187–198

    Article  Google Scholar 

  • Vigliotta G, Matrella S, Cicatelli A, Guarino F, Castiglione S (2016) Effects of heavy metals and chelants on phytoremediation capacity and on rhizobacterial communities of maize. J Environ Manag 179:93–102

    Article  CAS  Google Scholar 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining organic carbon in soils: effect of variations in digestion conditions and of inorganic soil constituents. Soil Scien 63:251–263

    Article  Google Scholar 

  • Wibberg D, Blom J, Jaenicke S, Kollin F, Rupp O, Scharf B et al (2011) Complete genome sequencing of Agrobacterium sp H13-3, the former Rhizobium lupini H13-3, reveals a tripartite genome consisting of a circular and a linear chromosome and an accessory plasmid but lacking a tumor-inducing Ti-plasmid. J Biotech 155:50–62

    Article  CAS  Google Scholar 

  • Wyszkowska J, Borowik A, Kucharski M, Kucharski J (2013) Effect of cadmium, copper and zinc on plants, soil microorganisms and soil enzymes. J Element 18:769–796

    Google Scholar 

  • Yang L, Wang G, Cheng Z, Liu Y, Shen Z, Luo C (2013) Influence of the application of chelant EDDS on soil enzymatic activity and microbial community structure. JHazar Mat 262:561–570

    Article  CAS  Google Scholar 

  • Yen JY, Broadway KM, Scharf BE (2012) Minimum requirements of flagellation and motility for infection of Agrobacterium sp strain H13-3 by flagellotropic bacteriophage 7-7-1. Appl Environ Microbiol 78:7216–7222

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by funds for didactic activity attributed to the course in “Applied Biology and Biodiversity” by the University of Salerno (University degree in Environmental Sciences) and by funds from the FARB project (2013) of the University of Salerno. We also acknowledge Elizabeth Illingworth for the English revision of the manuscript and Giovanni Vigliotta for bacterial strain isolation and MIC determination.

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Authors and Affiliations

  1. Dipartimento di Chimica e Biologia “A. Zambelli”, Università di Salerno, Fisciano, 84084, Salerno, Italy

    Angela Cicatelli, Francesco Guarino & Stefano Castiglione

  2. Dipartimento di Biologia, Università di Padova, 35131, Padova, Italy

    Enrico Baldan

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  1. Angela Cicatelli
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  2. Francesco Guarino
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  3. Enrico Baldan
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  4. Stefano Castiglione
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Correspondence to Stefano Castiglione.

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The original publication of this paper contains a mistake. Author names were inadvertently interchanged.

An erratum to this article is available at http://dx.doi.org/10.1007/s11356-017-8578-4.

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Cicatelli, A., Guarino, F., Baldan, E. et al. Genetic and biochemical characterization of rhizobacterial strains and their potential use in combination with chelants for assisted phytoremediation. Environ Sci Pollut Res 24, 8866–8878 (2017). https://doi.org/10.1007/s11356-016-7982-5

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