Skip to main content
SpringerLink
Log in

Study on cellular changes and potential endotrophy of wheat roots due to colonization of Chromium reducing bacteria

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

Chromium is a highly toxic metal for all living organisms. Industrial use of chromium has resulted in serious widespread pollution. Biological treatment (bioremediation) has proven to be a cost-effective option for cleanup of metal-contaminated sites. Several bacteria and plant species are able to tolerate high levels of chromium compounds that can be used for cleanup. An experiment was designed to study the colonization behavior of two indigenous Cr(VI)-reducing bacterial strain Pseudomonas aeruginosa Rb-1 and Ochrobactrum intermedium Rb-2 that were grown in wheat system amended with and without Cr(VI). Hydroponically grown wheat seedlings were co-inoculated with bacterial cultures to study the root colonization potential by fluorescent and electron microscopy. Bacterial inoculation caused significant increase in the growth of seedlings under Cr(VI) stress. Fluorescent microscopy showed good colonization potential of both bacterial strains with roots of inoculated seedlings. Electron micrographs revealed that Rb-1 tended to accumulate in the form of clusters, while Rb-2 preferred to be attach in groups of two or three cells to the root surface of inoculated seedlings. Chromium stress led to the elongation of bacterial rods along with uneven cell surface due to wrapping of cells in mucilaginous material. Cr(VI) stress also resulted in the damaging of plant root surface. Hence, few cells of Rb-2 entered the damaged root cortex cells and appeared as endophytes. Excessive production of fibrillar material by both bacteria under chromium stress could clearly be observed. Both strains displayed auxin production and Cr(VI) reduction ability, showing promise for bioremediation purposes.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahmed M, Stal LJ, Hasnain S (2010) Association of non-heterocystous cyanobacteria with crop plants. Plant Soil 336:363–375

    Article  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  Google Scholar 

  • Batool R, Yrjala K, Hasnain S (2012) Hexavalent chromium reduction by bacteria from tannery effluent. J Microbiol Biotechnol 22:547–554

    Article  CAS  Google Scholar 

  • Camargo FA, Okeke BC, Bento FM, Frankenberger WT (2003) In vitro reduction of hexavalent chromium by a cell free extract of Bacillus sp. ES 29 stimulated by Cu(2+). Appl Microbiol Biotechnol 62:569–573

    Article  CAS  Google Scholar 

  • Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  CAS  Google Scholar 

  • Cheung KH, Gu J-D (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59:8–15

    Article  CAS  Google Scholar 

  • Chukwuma SE, Richard T, Ephraim NA, Obinna AO, Ikechukwu NEO (2012) Biotechnological tools for environmental sustainability: prospects and challenges for environments in Nigeria—a standard review. Biotechnol Res Int. doi:10.1155/2012/450802

    Google Scholar 

  • Clesceri LS, Greenberg AE, Eaton AD (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington, p 1325. ISBN 087553235

  • Congeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146:270–277

    Article  CAS  Google Scholar 

  • De Jong W, Wösten HAB, Dijkhuizen L, Claessen D (2009) Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Mol Microbiol 73:1128–1140

    Article  Google Scholar 

  • Dimkpa C, Weinand T, Asch F (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    Article  CAS  Google Scholar 

  • Dowine JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170

    Article  Google Scholar 

  • Faisal M, Hasnain S (2003) Synergistic removal of Cr(VI) by Eichornia crassipes in conjunction with bacterial strains. Pak J Biol Sci 6:264–268

    Article  Google Scholar 

  • Faisal M, Hasnain S (2005) Chromate resistant Bacillus cereus augments sunflower growth by reducing toxicity of Cr(VI). J Plant Biol 48:187–194

    Article  CAS  Google Scholar 

  • Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of maize. Int J Biol Life Sci 49:19–24

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    CAS  Google Scholar 

  • Greer-Phillips SE, Stephens BB, Alexandre G (2004) An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 186:6595–6604

    Article  CAS  Google Scholar 

  • Hasnain S, Sabri AN (1997) Growth stimulation of Triticum aestivum seedlings under Cr-stresses by non rhizospheric Pseudomonad strains. Environ Poll 97(3):265–273

    Article  CAS  Google Scholar 

  • Hassen AI, Labuschagne N (2010) Root colonization and growth enhancement in wheat and tomato by rhizobacteria isolated from the rhizoplane of grasses. World J Microbiol Biotechnol 26:1837–1846

    Article  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19

    Article  Google Scholar 

  • Kim SJ, Kremer RJ (2005) Scanning and transmission electron microscopy of root colonization of morning-glory (Ipomoea spp.) seedlings by rhizobacteria. Symbios 39:117–124

    Google Scholar 

  • Li Y, Dick WA, Tuovinen OH (2004) Fluorescence microscopy for visualization of soil microorganisms—a review. Biol Fertil Soils 39:301–311

    Article  Google Scholar 

  • Lounatmaa K (1985) Electron microscopic methods for the study of bacterial surface structures. In: Korhonen TK, Dawes EA, Mäkelä PH (eds) Enterobacterial surface antigens: methods for molecular characterization. Elsevier Science Ltd, USA, pp 243–261

    Google Scholar 

  • Middleton SS, Latmani RB, Mackey MR, Ellisman MH, Tebo BM, Criddle CS (2003) Co-metabolism of Cr(VI) by Shewanella oneidensis MR-1 produces cell associated reduced chromium and inhibits growth. Biotechnol Bioeng 83:627–637

    Article  CAS  Google Scholar 

  • Molina MA, Ramos JL, Espinosa-Urgel M (2003) Plant-associated biofilms. Rev Environ Sci Technol 2:99–108

    Google Scholar 

  • Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41:429–453

    Article  CAS  Google Scholar 

  • Mukhopadhyay N, Aery NC (2000) Effect of Cr(III) and Cr(VI) on the growth and physiology of Triticum aestivum plants during early seedling growth. Biol Bratisl 55:403–408

    CAS  Google Scholar 

  • Rai AN, Soderback E, Bergman B (2000) Cyanobacterium-plant symbiosis. New Phytol 147:449–481

    Article  CAS  Google Scholar 

  • Rajkumar M, Nagendaran R, Lee KJ, Lee WH (2005) Characterization of a novel Cr6+ reducing Pseudomonas sp. with plant growth-promotion potential. Curr Microbiol 50:266–271

    Article  CAS  Google Scholar 

  • Sala VMR, Cardoso EJBN, Garboggini FF, Nogueira ND, da Silveira APD (2008) Achromobacter insolitus and Zoogloea ramigera associated with wheat plants (Triticum aestivum). Biol Fertil Soils 44:1107–1112

    Article  Google Scholar 

  • Santaella C, Schue M, Berge O, Heulin T, Achouak W (2008) The exopolysaccharide of Rhizobium sp. YAS34 is not necessary for biofilm formation on Arabidopsis thaliana and Brassica napus roots but contributes to root colonization. Environ Microbiol 10:2150–2163

    Article  CAS  Google Scholar 

  • Shahab S, Ahmed N, Khan NS (2009) Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs. Afr J Agric Res 4:1312–1316

    Google Scholar 

  • Souissi T, Kremer RJ, White JA (1997) Scanning and transmission electron microscopy of root colonization of leafy spurge (Euphorbia esula L.) seedlings by rhizobacteria. Phytomorphology 47:177–193

    Google Scholar 

  • Srinath T, Verma T, Ramteke PW, Garg SK (2002) Chromium (VI) biosorption and bioaccumulation by chromate resistant bacteria. Chemosphere 48:427–435

    Article  CAS  Google Scholar 

  • Subramaniam S, Balasubramaniam V, Poobathy R, Sreenivasan S, Rathinam X (2009) Chemotaxis movement and attachment of Agrobacterium tumefaciens to Phalaenopsis violacea orchid tissues: an assessment of early factors influencing the efficiency of gene transfer. Trop Life Sci Res 20:39–49

    Google Scholar 

  • Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T, Nevo E (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6:e17968. doi:10.1371/journal.pone.0017968

    Article  CAS  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2005) Auxin production by bacteria associated with orchid roots. Microbiology 74:46–53

    Article  CAS  Google Scholar 

  • US EPA (1998) Toxicological review of hexavalent chromium (CAS No 18540-29-9). In: Support of summary information on the integrated risk information system (IRIS). US Environmental Protection Agency, DC, Washington

  • Wani PA, Zaidi A, Khan MS (2009) Chromium reducing and plant growth promoting potential of Mesorhizobium species under chromium stress. Bioremediat J 13:121–129

    Article  CAS  Google Scholar 

  • World Health Association (1993) Guidelines for drinking-water quality, 2nd edn. ISBN 9241544600 (v.1) (NLM Classification: WA 675)

  • Yao J, Allen C (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol 188:3697–3708

    Article  CAS  Google Scholar 

  • Yaryura PM, Leon M, Correa OS, Kerber NL, Pucheu NL, Garcia AF (2008) Assessment of the role of chemotaxis and biofilm formation as requirements for colonization of roots and seeds of soybean plants by Bacillus amyloliquefaciens BNM339. Curr Microbiol 56:625–632

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Higher Education Commission of Pakistan is acknowledged for providing funding (IRSIP No. 1-8/HEC/HRD/2009/557) to visit the MEM-group at the Faculty of Biological and Environmental Sciences, Department of Biosciences, University of Helsinki, Finland. We thank Kari Lounatmaa for his assistance with SEM and TEM.

Author information

Authors and Affiliations

  1. Department of Microbiology and Molecular Genetics, University of the Punjab, Quaid-e-Azam Campus, Lahore, 54590, Pakistan

    R. Batool & S. Hasnain

  2. MEM-group, Department of Biosciences, University of Helsinki, Helsinki, Finland

    R. Batool & K. Yrjälä

Authors
  1. R. Batool
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Yrjälä
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Hasnain
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Batool.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Batool, R., Yrjälä, K. & Hasnain, S. Study on cellular changes and potential endotrophy of wheat roots due to colonization of Chromium reducing bacteria. Int. J. Environ. Sci. Technol. 12, 3263–3272 (2015). https://doi.org/10.1007/s13762-015-0757-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-015-0757-6

Keywords

Search

Navigation