Skip to main content
SpringerLink
Log in

Visualisation of gradients in arsenic concentrations around individual roots of Zea mays L. using agar-immobilized bioreporter bacteria

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The classical concept of arsenic transfer into plants through arsenate uptake via phosphate transporters, reduction to arsenite, complexation and compartmentation within vacuoles is challenged by recent identification of bidirectional transporters for arsenite and their potential role in plant As status regulation. Soil-based studies with chemical analysis of soil solution require root mat formation amplifying root effects on their surroundings and additionally denying investigations along individual roots differing in age and function. We tried to overcome these shortcomings by using bioreporter bacteria to visualise the spatial distribution of inorganic arsenic along roots and to characterize inorganic arsenic gradients in the rhizosphere concurrent with root age and branching. Therefore we developed an agar-based carrier element ensuring intimate contact between bioreporters and root-soil system and enabling fast and easy reporter output analysis. We show that inorganic arsenic distribution is related to root development with the highest bioreporter signal induction around lateral roots, which are known to show the highest expression of transporters responsible for bidirectional arsenite flux. Since there is so far no evidence for an arsenate efflux mechanism this is a strong indicator that we observed rather arsenite than arsenate efflux. No signal was detected along the distal region of young adventitious roots, i.e. the region of extension growth and root hair formation. The novel bioreporter assay may thus complement conventional measurements by providing information on the spatial distribution of inorganic arsenic on mm to cm-scale.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with imageJ. Biophot Int 11:36–42

    Google Scholar 

  • Ackermann J, Vetterlein D, Tanneberg H, Neue H-U, Mattusch J, Jahn R (2008) Speciation of arsenic under dynamic conditions. Eng Life Sci 8:589–597

    Article  CAS  Google Scholar 

  • Ackermann J, Vetterlein D, Kaiser K, Mattusch J, Jahn R (2009) The bioavailability of arsenic in floodplain soils—a simulation of water saturation. EJSS-315-08

  • Belkin S (2003) Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 6:206–212

    Article  CAS  PubMed  Google Scholar 

  • Bienert GP, Schuessler MD, Jahn TP (2008) Metalloids: essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem Sci 33:20–26

    Article  CAS  PubMed  Google Scholar 

  • Bleeker PM, Hakvoort HWJ, Bliek M, Souer E, Schat H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant Journal 45:917–929

    Article  CAS  PubMed  Google Scholar 

  • Bravin M, Travassac F, Le Floch M, Hinsinger P, Garnier J-M (2008) Oxygen input controls the spatial and temporal dynamics of arsenic at the surface of a flooded paddy soil and in the rhizosphere of lowland rice (Oryza sativa L.): a microcosm study. Plant Soil 312:207–218

    Article  CAS  Google Scholar 

  • Burgess SSO, Bleby TM (2006) Redistribution of soil water by lateral roots mediated by stem tissues. J Exp Bot 57:3283–3291

    Article  CAS  PubMed  Google Scholar 

  • Cardon ZG, Gage DJ (2006) Resource exchange in the rhizosphere: molecular tools and the microbial perspective. Annu Rev Ecol Evol Syst 37:459–488

    Article  Google Scholar 

  • Clarkson DT (1991) Root structure and site of ion uptake. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, Inc. New York, pp 417–453

    Google Scholar 

  • Darwent MJ, Paterson E, McDonald AJS, Tomos AD (2003) Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration. J Exp Bot 54:325–334

    Article  CAS  PubMed  Google Scholar 

  • Daunert S, Barrett G, Feliciano JS, Shetty RS, Shrestha S, Smith-Spencer W (2000) Genetically engineered whole-cell sensing systems: coupling biological recognition with reporter genes. Chem Rev 100:2705–2738

    Article  CAS  PubMed  Google Scholar 

  • DeAngelis KM, Ji PS, Firestone MK, Lindow SE (2005) Two novel bacterial biosensors for detection of nitrate availability in the rhizosphere. Appl Environ Microbiol 71:8537–8547

    Article  CAS  PubMed  Google Scholar 

  • Delnomdedieu M, Basti MM, Otvos JD, Thomas DJ (1994) Reduction and binding of arsenate and dimethylarsinate by glutathione: a magnetic resonance study. Chem Biol Interact 90:139–155

    Article  CAS  PubMed  Google Scholar 

  • Ernst M, Römheld V, Marschner H (1989) Estimation of phosphorus uptake capacity by different zones of the primary root of soil-grown maize (Zea mays L.). J Plant Nut Soil Sci 152:21–25

    Article  CAS  Google Scholar 

  • Fitz WJ, Wenzel WW, Zhang H, Nurmi J, Stipek K, Fischerova Z, Schweiger P, Kollensperger G, Ma LQ, Stingeder G (2003) Rhizosphere characteristics of the arsenic hyperaccumulator Pteris vittata L. and monitoring of phytoremoval efficiency. Environ Sci Technol 37:5008–5014

    Article  CAS  PubMed  Google Scholar 

  • Gantner S, Schmid M, Dürr C, Schuhegger R, Steidle A, Hutzler P, Langebartels C, Eberl L, Hartmann A, Dazzo FB (2006) In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol Ecol 56:188–194

    Article  CAS  PubMed  Google Scholar 

  • Geelhoed JS, Hiemstra T, Van Riemsdijk WH (1998) Competitive interaction between phosphate and citrate on goethite. Environ Sci Technol 32:2119–2123

    Article  CAS  Google Scholar 

  • Goldberg S, Glaubig RA (1988) Anion sorption on a calcareous, montmorillonitic soil arsenic. Soil Sci Soc Am J 52:1297–1300

    CAS  Google Scholar 

  • Grafe M, Eick MJ, Grossl PR (2001) Adsorption of arsenate (V) and arsenite (III) on goethite in the presence and absence of dissolved organic carbon. Soil Sci Soc Am J 65:1680–1687

    CAS  Google Scholar 

  • Gulz PA, Gupta S-K, Schulin R (2005) Arsenic accumulation of common plants from contaminated soils. Plant Soil 272:337–347

    Article  CAS  Google Scholar 

  • Harms H, Rime J, Leupin O, Hug SJ, van der Meer JR (2005) Effect of groundwater composition on arsenic detection by bacterial biosensors. Microchim Acta 151:217–222

    Article  CAS  Google Scholar 

  • Harms H, Wells MC, van der Meer JR (2006) Whole-cell living biosensors—are they ready for environmental application? Appl Environ Biotechnol 70:273–280

    CAS  Google Scholar 

  • Hinsinger P, Bengough A, Vetterlein D, Young I (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil. doi:10.1007/s11104-008-9885-9

    Google Scholar 

  • Ivask A, Virta M, Kahru A (2002) Construction and use of specific luminescent recombinant bacterial sensors for the assessment of bioavailable fraction of cadmium, zinc, mercury and chromium in the soil. Soil Biol Biochem 34:1439–1447

    Article  CAS  Google Scholar 

  • Leveau JHJ, Lindow SE (2002) Bioreporters in microbial ecology. Curr Opin Microbiol 5:259–265

    Article  PubMed  Google Scholar 

  • Liu F, De Cristofaro A, Violante A (2001) Effect of pH, phosphate and oxalate on the adsorption/desorption of arsenate on/from goethite. Soil Science 166:197–208

    Article  CAS  Google Scholar 

  • Livesey NT, Huang PM (1981) Adsorption of arsenate by soils and its relation to selected chemical-properties and anions. Soil Science 131:88–94

    Article  CAS  Google Scholar 

  • Ma JF, Goto S, Tamai K, Ichii M (2001) Role of root hairs and lateral roots in silicon uptake by rice. Plant Physiol 127:1773–1780

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu X-Y, Su Y-H, McGrath SP, Zhao F-J (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935

    Article  CAS  PubMed  Google Scholar 

  • Masscheleyn PH, Delaune RD, Patrick WH (1991) Effect of redox potential and pH on arsenic speciation and solubility in a contaminated soil. Environ Sci Technol 25:1414–1419

    Article  CAS  Google Scholar 

  • Mimura T (1999) Regulation of phosphate transport and homeostasis in plant cells. Int Rev Cytol 191:149–200

    Article  CAS  Google Scholar 

  • Mitani N, Yamaji N, Ma JF (2009) Identification of maize silicon influx transporters. Plant Cell Physiol 50:5–12

    Article  CAS  PubMed  Google Scholar 

  • Morin G, Calas G (2006) Arsenic in soils, mine tailings, and former industrial sites. Elements 2:97–101

    Article  CAS  Google Scholar 

  • Nordstrom DK (2002) Public health—worldwide occurrences of arsenic in groundwater. Science 296:2143–2145

    Article  CAS  PubMed  Google Scholar 

  • Paitan Y, Biran I, Shechter N, Biran D, Rishpon J, Ron EZ (2004) Monitoring aromatic hydrocarbons by whole cell electrochemical biosensors. Anal Biochem 335:175–183

    Article  CAS  PubMed  Google Scholar 

  • Paterson E, Sim A, Standing D, Dorward M, McDonald AJS (2006) Root exudation from Hordeum vulgare in response to localised nitrate supply. J Exp Bot 57:2413–2420

    Article  CAS  PubMed  Google Scholar 

  • Raab A, Williams PN, Meharg AA, Feldmann J (2007) Uptake and translocation of inorganic and methylated arsenic species by plants. Environ Chem 4:107–203

    Article  CAS  Google Scholar 

  • Ramanathan S, Shi WP, Rosen BP, Daunert S (1997) Sensing antimonite and arsenite at the subattomole level with genetically engineered bioluminescent bacteria. Anal Chem 69:3380–3384

    Article  CAS  PubMed  Google Scholar 

  • Römheld V, Müller C, Marschner H (1984) Localization and capacity of proton pumps in roots of intact sunflower plants. Plant Physiol 76:603–606

    Article  PubMed  Google Scholar 

  • Roy WR, Hassett JJ, Griffin RA (1986) Competitive coefficients for the adsorption of arsenate, molybdate and phosphate mixtures by soils. Soil Sci Soc Am J 50:1176–1182

    Article  CAS  Google Scholar 

  • Shin H, Shin H-S, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant Journal 39:629–642

    Article  CAS  PubMed  Google Scholar 

  • Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568

    Article  CAS  Google Scholar 

  • Smith E, Naidu R, Alston AM (1998) Arsenic in the soil environment: a review. Adv Agron 64:149–195

    Article  CAS  Google Scholar 

  • Stocker J, Balluch D, Gsell M, Harms H, Feliciano J, Daunert S, Malik KA, Van der Meer JR (2003) Development of a set of simple bacterial biosensors for quantitative and rapid measurements of arsenite and arsenate in potable water. Environ Sci Technol 37:4743–4750

    Article  CAS  PubMed  Google Scholar 

  • Szegedi K, Vetterlein D, Nietfeld H, Jahn R, Neue H-U (2008) The new tool RhizoMath for modeling coupled transport and speciation in the rhizosphere. Vadose Zone J, Special Issue “Vadose Zone Modeling” 7:712–720

    Google Scholar 

  • Trang PTK, Berg M, Viet PH, Mui NV, van der Meer JR (2005) Bacterial bioassay for rapid and accurate analysis of arsenic in highly variable groundwater samples. Environ Sci Technol 39:7625–7630

    Article  CAS  PubMed  Google Scholar 

  • van der Meer JR, Tropel D, Jaspers M (2004) Illuminating the detection chain of bacterial bioreporters. Environ Microbiol 6:1005–1020

    Article  PubMed  CAS  Google Scholar 

  • Vetterlein D, Szegedi K, Ackermann J, Mattusch J, Neue HU, Tanneberg H, Jahn R (2007) Competitive mobilization of phosphate and arsenate associated with goethite by root activity. J Environ Qual 36:1811–1820

    Article  CAS  PubMed  Google Scholar 

  • Wackwitz A, Harms H, Chatzinotas A, Breuer U, Vogne C, van der Meer JR (2008) Internal arsenite bioassay calibration using multiple bioreporter cell lines. Microbial Biotechnol 1:149–157

    Article  CAS  Google Scholar 

  • Welch AH, Westjohn DB, Helsel DR, Wanty RB (2000) Arsenic in ground water of the United States: occurrence and geochemistry. Ground Water 38:589–604

    Article  CAS  Google Scholar 

  • Wells M, Gosch M, Harms H, van der Meer JR (2005) Response characteristics of arsenic-sensitive bioreporters expressing the gfp reporter gene. Microchim Acta 151:209–216

    Article  CAS  Google Scholar 

  • Werlen C, Jaspers MCM, van der Meer JR (2004) Measurement of biologically available naphthalene in gas and aqueous phases by use of a Pseudomonas putida biosensor. Appl Environ Microbiol 70:43–51

    Article  CAS  PubMed  Google Scholar 

  • Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Environmental Microbiology, UFZ, Helmholtz Centre for Environmental Research, Permoserstrasse 15, 04318, Leipzig, Germany

    Anke Kuppardt, Hauke Harms & Antonis Chatzinotas

  2. Department of Soil Physics, UFZ, Helmholtz Centre for Environmental Research, 06120, Halle, Germany

    Doris Vetterlein

Authors
  1. Anke Kuppardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doris Vetterlein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hauke Harms
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antonis Chatzinotas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antonis Chatzinotas.

Additional information

Responsible editor: Philippe Hinsinger.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 6.03 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuppardt, A., Vetterlein, D., Harms, H. et al. Visualisation of gradients in arsenic concentrations around individual roots of Zea mays L. using agar-immobilized bioreporter bacteria. Plant Soil 329, 295–306 (2010). https://doi.org/10.1007/s11104-009-0154-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0154-3

Keywords

Search

Navigation