Skip to main content
Log in

Cadmium-tolerant bacteria induce metal stress tolerance in cereals

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Cadmium usually hampers plant growth, but bacterial inoculation may improve stress tolerance in plants to Cd by involving various mechanisms. The objective was to characterize and identify bacteria that improve plant growth under Cd stress and reduce Cd uptake. Cadmium-tolerant bacteria were isolated from rhizosphere soil, which was irrigated with tannery effluent, and six strains were selected as highly tolerant to Cd, showing minimum inhibitory concentration as 500 mg L−1 or 4.45 mmol L−1. These strains were identified by 16S rRNA gene analysis and functional analysis in regard to plant growth promotion characteristics. To determine their effect on cereal growth under Cd stress, seeds were inoculated with these strains individually and grown in soil contaminated with three Cd levels (0, 40 and 80 mg kg−1). Biomass production, relative water content (RWC), electrolyte leakage (ELL) and tissue Cd concentration were measured. Biomass of both cereals was inhibited strongly when exposed to Cd; however, bacterial inoculation significantly reduced the suppressive effect of Cd on cereal growth and physiology. The bacterial isolates belonged to the genera Klebsiella, Stenotrophomonas, Bacillus and Serratia. Maize was more sensitive than wheat to Cd. Klebsiella sp. strain CIK-502 had the most pronounced effects in promoting maize and wheat growth and lowering Cd uptake under Cd stress.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmad I, Akhtar MJ, Zahir ZA, Jamil A (2012) Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pak J Bot 44:1569–1574

    CAS  Google Scholar 

  • Ajaz haja mohideen R, Arasu VT, Narayanan KR, Hussain MIZ (2010) Bioremediation of heavy metal contaminated soil by the Exiguobacterium and accumulation of Cd, Ni, Zn and Cu from soil environment. Int J Biol Technol 1:94–101

    Google Scholar 

  • Alami Y, Achouk W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398

    Article  CAS  Google Scholar 

  • Alloway BJ (1995) Heavy metals in soil. Blackie Academic and Professional, London

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brown CM, Dilworth MJ (1975) Ammonia assimilation by rhizobium cultures and bacteroids. J Gen Microbiol 122:61–67

    Google Scholar 

  • Cassana F, Perriga D, Sgroya V, Masciarellia O, Pennab C, Lunaa V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E 109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L) and soybean (Glycine max L). Eur J Soil Biol 45:28–35

    Article  Google Scholar 

  • Chen S, Chao L, Sun L, Sun T (2013) Effects of bacteria on cadmium bioaccumulation in the cadmium hyperaccumulator plant Beta vulgaris var. Cicla L. Int J Phytorem 15:477–487

    Article  CAS  Google Scholar 

  • Dimkpa CO, Merten D, Svatos A, Buchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162

    Article  CAS  Google Scholar 

  • Dodd IC, Belimov AA, Sobeih WY, Safronova VI, Grierson D, Davies WJ (2010) Will modifying plant ethylene status improve plant productivity in water limited environments? In: New directions for a diverse planet: Proc. Int. Crop Sci. Congr., 4th, Brisbane, Australia, 26 September - 1 October 2004, Available at www.cropscience.org.au/icsc2004/poster/1/3/4/510doddicref.htm (verified 10 January 2010). Regional Inst., Gosford, NSW, Australia

  • Dourado MN, Martins PF, Quecine MC, Piotto FA, Souza LA, Franco MR, Tezotto T, Azevedo RA (2013) Burkholderia sp. SCMS54 reduces cadmium toxicity and promotes growth in tomato. Ann Appl Biol 163:494–507

    CAS  Google Scholar 

  • Edwards U, Rogall T, Blocker H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853

    Article  CAS  Google Scholar 

  • Ekmekci Y, Tanyolac D, Ayhan B (2009) A crop tolerating oxidative stress induced by excess lead: maize. Acta Physiol Plant 31:319–330

    Article  CAS  Google Scholar 

  • Farwell AJ, Vesely S, Nero V, Rodriguez H, McCormack K, Shah S, Dixon DG, Glick BR (2007) Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal-contaminated field site. Environ Pollut 147:540–545

    Article  CAS  Google Scholar 

  • Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119

    Article  CAS  Google Scholar 

  • Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guo M, Block A, Bryan CD, Becker DF, Alfano JR (2012) Pseudomonas syringae catalases are collectively required for plant pathogenesis. J Bacteriol 194:5054–5064

    Article  CAS  Google Scholar 

  • Hussain MB, Zahir ZA, Asghar HN, Asghar M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int J Agric Biol 16:3–13

    CAS  Google Scholar 

  • Iram S, Ahmad I, Akhtar S (2012) Distribution of heavy metals in peri-urban agricultural areas soils. J Chem Soc Pak 34:861–869

    CAS  Google Scholar 

  • Karimzadeh L, Heilmeier H, Merkel BJ (2012) Effect of microbial siderophore DFO-B on Cd accumulation by Thlaspi caerulescens hyperaccumulator in the presence of zeolite. Chemosphere 88:683–687

    Article  CAS  Google Scholar 

  • Khan AL, Lee IJ (2013) Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol 13:86–100

    Article  CAS  Google Scholar 

  • Kovács N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature (London) 178:703

    Article  Google Scholar 

  • Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A (2008) Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304:35–44

    Article  CAS  Google Scholar 

  • Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484

    Article  CAS  Google Scholar 

  • Lasat HA (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31(1):109–120

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L). Chemosphere 69:220–228

    Article  CAS  Google Scholar 

  • Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278

    Article  CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance in tomato and pepper plants to salt stress. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739

    Article  CAS  Google Scholar 

  • Murtaza G, Ghafoor A, Qadir MJ (2008) Accumulation and implications of cadmium, cobalt and manganese in soils and vegetables irrigated with city effluent. J Sci Food Agric 88(1):100–107

    Article  CAS  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc Am J 74:533–542

    Article  Google Scholar 

  • Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A (2013) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils. doi:10.1007/s00374-013-0854-y

    Google Scholar 

  • Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39

    Article  CAS  Google Scholar 

  • Nicolaus B, Lama L, Esposito E, Manca MC, Improta R, Bellitti MR, Duckworth AW, Grant WD, Gambacorta A (1999) Haloarcula spp. able to biosynthesize exo- and endopolymers. J Ind Microbiol Biotechnol 23:489–496

    Article  CAS  Google Scholar 

  • Paul D, Nair S (2008) Stress adaptations in a plant growth promoting rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J Basic Microbiol 48:378–384

    Article  CAS  Google Scholar 

  • Prapagdee B, Watcharamusik A (2009) Adaptive and cross-protective responses against cadmium and zinc toxicity in cadmium-resistant bacterium isolated from a zinc mine. Braz J Microbiol 40:838–845

    Article  CAS  Google Scholar 

  • Reichman SM, Parker DR (2005) Metal complexation by phytosiderophores in the rhizosphere. Biogeochemistry of trace elements in the rhizosphere. Elsevier, New Jersey

    Google Scholar 

  • Rojas-Tapias D, Moreno-Galván A, Pardo-Díaz S, Obando M, Rivera D, Bonilla R (2012) Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl Soil Ecol 61:264–272

    Article  Google Scholar 

  • Sarwar M, Arshad M, Martens DA, Frankenberger WT Jr (1992) Tryptophan dependent biosynthesis of auxins in soil. Plant Soil 147:207–215

    Article  CAS  Google Scholar 

  • Schwager S, Lumjiaktase P, Stockli M, Weisskopf L, Eberl L (2012) The genetic basis of cadmium resistance of Burkholderia cenocepacia. Environ Microbiol Rep 4:562–568

    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, Puschenreiter M (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 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press Inc., San Diego

    Google Scholar 

  • Vanderlinde EM, Harrison JJ, Muszynski A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC-transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340

    Article  CAS  Google Scholar 

  • Vangronsveld J, Cunningham SD (1998) Introduction to the concepts. In: Vangronsveld J (ed) Metal-contaminated soils: in-situ inactivation and phytorestoration. Springer, Berlin, pp 1–15

    Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnelajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  CAS  Google Scholar 

  • Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes and antioxidant status of maize under drought stress. J Plant Interact 6:1–14

    Article  CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 43:1691–1705

    Google Scholar 

  • Yang Y, Zhang F, Li H, Jiang R (2009) Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils. J Environ Manag 90:1117–1122

    Article  CAS  Google Scholar 

  • Zhang S, Li T, Huang H, Zou T, Zhang X, Yu H, Zheng Z, Wang Y (2012) Cd accumulation and phytostabilization potential of dominant plants surrounding mining tailings. Environ Sci Pollut Res Int 9:3879–3888

    Article  Google Scholar 

Download references

Acknowledgments

The first author acknowledges the “Higher Education Commission (HEC) of Pakistan” to provide financial support for this project under the Indigenous 5000 Fellowship Scheme Batch IV.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Iftikhar Ahmad.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmad, I., Akhtar, M.J., Zahir, Z.A. et al. Cadmium-tolerant bacteria induce metal stress tolerance in cereals. Environ Sci Pollut Res 21, 11054–11065 (2014). https://doi.org/10.1007/s11356-014-3010-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3010-9

Keywords

Navigation