Skip to main content

Brevibacillus, Arbuscular Mycorrhizae and Remediation of Metal Toxicity in Agricultural Soils

  • Chapter
  • First Online:

Part of the book series: Soil Biology ((SOILBIOL,volume 27))

Abstract

Increasing industrial and anthropogenic activities have caused environmental pollution and have raised the concentrations of toxic metals in agricultural soils. Beneficial interactions between plants and rhizosphere microorganisms have been demonstrated to alleviate metal toxicity and nutrient deficiency. In fact, inoculation with heavy metal-resistant, rhizosphere bacteria isolated from metal-polluted soils have been shown to substantially improve plant growth and development under conditions of toxic metal pollution. This effect is even more evident if metal-resistant bacteria are co-inoculated with indigenous arbuscular mycorrhizal (AM) fungal strains. Thus, we need a better understanding of the interactions between beneficial microbes such as AM fungi and heavy metal-resistant rhizobacteria. This chapter summarizes the mechanisms involved in bioremediation of heavy metal-contaminated soils by studies involving co-inoculation of plants with autochthonous Brevibacillus and AM fungal strains isolated from heavy metal-polluted soils. The chapter also describes protocols for key methods in the study of such mechanisms.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aertsen A, Michiels CV (2005) Diversify or die: generation of diversity in response to stress. Crit Rev Microbiol 31:69–78

    Article  PubMed  Google Scholar 

  • Amoozegar MA, Hamedi J, Dadashipour M, Shariatpahahi S (2005) Effect of salinity on the tolerance to toxic metals and oxyanions in native moderately halophilic spore-forming bacilli. World J Microbiol Biotechnol 21:1237–1243

    Article  CAS  Google Scholar 

  • Ann ZQ, Hendrix JW, Hershman DE, Henson GT (1990) Evaluation of the “most probable number” (MPN) and wet-sieving methods for determining soil-borne populations of endogonaceous mycorrhizal fungi. Mycologia 82:516–518

    Article  Google Scholar 

  • Azcón R (1987) Germination and hyphal growth of Glomus mosseae in vitro: effects of rhizosphere bacteria and cell-free culture media. Soil Biol Biochem 19:417–419

    Article  Google Scholar 

  • Azcón R (1993) Growth and nutrition of nodulated mycorrhizal and non-mycorrhizal Hedysarum coronarium as a result of treatments with fractions from a plant growth-promoting rhizobacteria. Soil Biol Biochem 25:1037–1042

    Article  Google Scholar 

  • Azcón R, Medina A, Roldán A, Biró B, Vivas A (2009) Significance of treated agrowaste residue and autochthonous inoculates (arbuscular mycorrhizal fungi and Bacillus cereus) on bacterial community structure and phytoextraction to remediate soils contaminated with heavy metals. Chemosphere 75:327–334

    Article  PubMed  Google Scholar 

  • Barea JM, Tobar RM, Azcón-Aguilar C (1996) Effect of a genetically modified Rhizobium meliloti inoculant on the development of arbuscular mycorrhizas, root morphology, nutrient uptake and biomass accumulation in Medicago sativa. New Phytol 134:361–369

    Article  Google Scholar 

  • Beveridge TJ (1988) The bacterial surface: general considerations towards design and function. Can J Microbiol 34:363–372

    Article  PubMed  CAS  Google Scholar 

  • Biró B, Bayoumi HEAF, Balázsy S, Kecskés M (1995) Metal sensitivity of some symbiotic N2-fixing bacteria and Pseudomonas strains. Acta Biol Hung 46:9–16

    PubMed  Google Scholar 

  • Biró B, Köves-Péchy K, Vörösm I, Kádár I (1998) Toxicity of some field applied heavy metal salts to the rhizobial and fungal microsymbionts of alfalfa and red clover. Agrokém Talaj 47:265–276

    Google Scholar 

  • Bolan NS, Duraisamy VP (2003) Role of inorganic and organic soil amendments on immobilisation and phytoavailability of heavy metals: a review involving specific case studies. Aust J Soil Res 41:533–555

    Article  CAS  Google Scholar 

  • Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Adv Agron 66:1–102

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Burleigh SH, Bechmann IE (2002) Plant nutrient transporter regulation in arbuscular mycorrhizas. Plant Soil 244:247–251

    Article  CAS  Google Scholar 

  • Burleigh S, Kristensen BK, Bechmann IA (2003) Plasma membrane zinc transporter from Medicago truncatula is upregulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol Biol 52:1077–1088

    Article  PubMed  CAS  Google Scholar 

  • Chao CC, Wang YP (1990) Effects of heavy metals on the infection of vesicular arbuscular mycorrhizae and the growth of maize. J Agric Assoc China 153:34–45

    Google Scholar 

  • Charudhry TM, Hayes WJ, Khan AG, Khoo CS (1998) Phytoremediation-focusing on accumulator plants that remediate metal-contaminated soils. Aust J Ecotoxicol 4:37–51

    Google Scholar 

  • Chen BD, Li XL, Tao HQ, Christie P, Wong MH (2003) The role of arbuscular mycorrhizal in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846

    Article  PubMed  CAS  Google Scholar 

  • Crowley DE, Dungan RS (2002) Encyclopaedia of environmental microbiology, vol 4. Gabriel Bitton Wiley Interscience, New York, pp 1878–1892

    Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • García C, Hernández MT, Costa F (1997) Potential use of dehydrogenase activity as an index of microbial activity in degraded soils. Commun Soil Sci Plant Nutr 28:123–134

    Article  Google Scholar 

  • Giovannetti L, Ventura S, Bazzicalupo M, Fani R, Materassi R (1990) DNA restriction fingerprint analysis of the soil bacterium Azospirillum. J Gen Microbiol 136:1161–1166

    PubMed  CAS  Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fung Genet Biol 42:130–140

    Article  Google Scholar 

  • Gray JT, Schlesinger WH (1983) Nutrient use by evergreen and deciduous shrubs in Southern-California. 2. Experimental investigations of the relationship between growth, nitrogen uptake and nitrogen availability. J Ecol 71:43–56

    Article  CAS  Google Scholar 

  • Grichko VP, Filby B, Glick BR (2000) Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd, Co, Cu, Ni, Pb and Zn. J Biotechnol 81:45–53

    Article  PubMed  CAS  Google Scholar 

  • Gryndler M, Hrselová H, Stríteská D (2000) Effect of soil bacteria on hyphal growth of the arbuscular mycorrhizal fungus Glomus claroideum. Folia Microbiol 45:545–551

    Article  CAS  Google Scholar 

  • Hafeburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467

    Article  Google Scholar 

  • Hall JM (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • Hartley W, Eduards R, Lepp WN (2004) Arsenic and heavy metal mobility in iron oxide-amended contaminated soils as evaluated by short and long term leaching tests. Environ Pollut 131:495–504

    Article  PubMed  CAS  Google Scholar 

  • Hepper CM, Jakobsen I (1983) Hyphal growth from spores of the mycorrhizal fungus Glomus caledonius: effect of amino acids. Soil Biol Biochem 15:55–58

    Article  CAS  Google Scholar 

  • Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  • Kádár I (1995) Contamination of the soil–plant–animal–man foodchain by chemical elements in Hungary. Ministry of Environmental Protection and Land Management, Budapest (In Hungarian)

    Google Scholar 

  • Kanazawa S, Mori K (1996) Isolation of cadmium-resistant bacteria and their resistance mechanisms. Part II. Cadmium biosorption by Cd resistant and sensitive bacteria. Soil Sci Plant Nutr 42:731–736

    CAS  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizosphere of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  PubMed  CAS  Google Scholar 

  • Kinkle BK, Sadowsky MJ, Johanstone K, Koskinen WC (1994) Tellurium and selenium resistance in Rhizobia and its potential use for direct isolation of Rhizobium meliloti from soil. Appl Environ Microbiol 60:1674–1677

    PubMed  CAS  Google Scholar 

  • Kloepper JW (1992) Plant growth-promoting rhizobacteria as biological control agents. In: Blaine F, Metting J Jr (eds) Applications in agriculture forestry and environmental management. Marcel Dekker, New York, pp 255–274

    Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–147

    Google Scholar 

  • Leyval C, Turnau K, Haslwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153

    Article  CAS  Google Scholar 

  • Li XL, Christie P (2001) Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 42:201–207

    Article  PubMed  CAS  Google Scholar 

  • Märtensson AM (1992) Effects of agrochemicals and heavy metals on fast-growing rhizobia and their symbiosis with small-seeded legumes. Soil Biol Biochem 24:435–445

    Article  Google Scholar 

  • Masciandaro G, Ceccanti B, García C (1994) Anaerobic digestion of straw and piggery wastewater: II. Optimization of the process. Agrochimica 3:195–203

    Google Scholar 

  • Medina A, Vassilev N, Alguacil MM, Roldán A, Azcón R (2004) Increased plant growth, nutrient uptake, and soil enzymatic activities in a desertified Mediterranean soil amended with treated residues and inoculated with native mycorrhizal fungi and a plant growth-promoting yeast. Soil Sci 169:260–270

    Article  CAS  Google Scholar 

  • Medina A, Vassileva M, Barea JM, Azcón R (2006) The growth enhancement of clover by Aspergillus-treated sugar beet waste and Glomus mosseae inoculation in Zn contaminated soil. Appl Soil Ecol 33:87–98

    Article  Google Scholar 

  • Mercier G, Duchesne J, Carles-Gibergues A (2002) A simple and fast screening test to detect soils polluted by lead. Environ Pollut 118:285–296

    Article  PubMed  CAS  Google Scholar 

  • Meyer JR, Linderman RG (1986) Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungia and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol Biochem 18:185–190

    Article  CAS  Google Scholar 

  • Mosse B (1962) The establishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J Gen Microbiol 27:509–520

    PubMed  CAS  Google Scholar 

  • Mullen MD, Wolf DC, Gerris FG, Beveridge TJ, Flemming CA, Bailey GW (1989) Bacterial sorption of heavy metals. Appl Environ Microbiol 55:3143–3149

    PubMed  CAS  Google Scholar 

  • Mulligan CN, Yong RN, Gibs BF (2001) Remediation technologies for metal-contaminated soils and groundwater: an evaluation. Eng Geol 60:193–207

    Article  Google Scholar 

  • Naseby DC, Lynch JM (1997) Rhizosphere soil enzymes as indicators of perturbation caused by a genetically modified strain of Pseudomonas fluorescens on wheat seed. Soil Biol Biochem 29:1353–1362

    Article  CAS  Google Scholar 

  • Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199

    Article  PubMed  CAS  Google Scholar 

  • Nishimura K, Igarashi K, Kakinuma Y (1998) Protongradient-driven nickel uptake by vacuolar membrane vesicles of Saccharomyces cerevisiae. J Bacteriol 180:1962–1964

    PubMed  CAS  Google Scholar 

  • Paulsen IT, Saier MH Jr (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156:99–103

    Article  PubMed  CAS  Google Scholar 

  • Pichtel J, Kuroiwa K, Sawyerr HT (2000) Distribution of Pb, Cd and Ba in soils and plants of two contaminated sites. Environ Pollut 110:171–178

    Article  PubMed  CAS  Google Scholar 

  • Pishchik VN, Vorobyev NI, Chernyaeva LL, Timofeeva SV, Kozhemyakov AP, Alexeev YV, Lukin SM (2002) Experimental and mathematical simulation of plant growth promoting rhizobacteria and plant interaction under cadmium stress. Plant Soil 243:173–186

    Article  CAS  Google Scholar 

  • Rajkumar M, Ma Y, Freitas H (2008) Characterization of metal-resistant plant-growth promoting Bacillus weihenstephanensis isolated from serpentine soil in Portugal. J Basic Microbiol 18:500–508

    Article  Google Scholar 

  • Requena N, Jimenez I, Toro M, Barea JM (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136:667–677

    Article  Google Scholar 

  • Roldán A, Albaladejo J, Thornes J (1996) Aggregate stability changes in a semiarid soil after treatment with different organic amendments. Arid Soil Res Rehabil 10:139–148

    Google Scholar 

  • Scholeske S, Maetz M, Schneider T, Hildebrandt U, Bothe H, Povh B (2004) Element distribution in mycorrhizal and non-mycorrhizal roots of the halophyte Aster tripolium determined by proton induced X-ray emission. Protoplasma 223:183–189

    Google Scholar 

  • Sheng XF, Xia JJ (2006) Improvement of rape (Brasica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64:1036–1042

    Article  PubMed  CAS  Google Scholar 

  • Shetty KG, Banks MK, Hetrick BA, Schwab AP (1994a) Biological characterization of a southeast Kansas mining site. Water Air Soil Pollut 78:169–177

    Article  CAS  Google Scholar 

  • Shetty KG, Hetrick BAD, Figge DAH, Schwab AP (1994b) Effects of mycorrhizae and other soil microbes on revegetation of heavy metal contaminated mine spoil. Environ Pollut 86:181–188

    Article  PubMed  CAS  Google Scholar 

  • Simon L, Szegvári I, Prokisch J (2001) Enhancement of chromium phytoextraction capacity in fodder radish with pycolinic acid. Environ Geochem Health 23:313–316

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Tabak H, Lens P, van Hullebusch ED, Dejonghe W (2005) Development in bioremediation of soils and sediments polluted with metals and radionuclides – 1. Microbial processes and mechanisms affecting bioremediation of metal contamination and influencing metal toxicity and transport. Rev Environ Sci Biotechnol 4:115–156

    Article  CAS  Google Scholar 

  • Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller EM, Keeney DR (eds) Methods of soil analysis, part 2, 2nd edn. Agronomy Monograph 9. ASA and SSSA, Madison, WI, pp 501–538

    Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria from the remediation of heavy metal pollutions. FEMS Microbiol Rev 26:327–338

    PubMed  CAS  Google Scholar 

  • Vivas A, Azcón R, Biró B, Barea JM, Ruíz-Lozano JM (2003a) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol 49:577–588

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Biró B, Campos E, Barea JM, Azcón R (2003b) Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp isolated from cadmium polluted soil under increasing cadmium levels. Environ Pollut 126:179–189

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Vörös I, Biró B, Barea JM, Ruíz-Lozano JM, Azcón R (2003c) Beneficial effects of indigenous Cd-tolerant and Cd-sensitive Glomus mosseae associated with a Cd-adapted strain of Brevibacillus sp. in improving plant tolerance to Cd contamination. Appl Soil Ecol 24:177–186

    Article  Google Scholar 

  • Vivas A, Barea JM, Azcón R (2005a) Brevibacillus brevis isolated from cadmium or zinc contaminated soils improves in vitro spore germination and growth of Glomus mosseae under high Cd or Zn concentrations. Microb Ecol 49:416–424

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Barea JM, Azcón R (2005b) Interactive effect of Brevibacillus brevis and Glomus mosseae, both isolated from Cd contaminated soil, on plant growth, physiological mycorrhizal fungal characteristics and soil enzymatic activities in Cd-polluted soil. Environ Pollut 134:257–266

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Barea JM, Biró B, Azcón R (2006a) Effectiveness of authochthonous bacterium and mycorrhizal fungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminated soil. J Appl Microbiol 100:587–598

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Biró B, Németh T, Barea JM, Azcón R (2006b) Nickel-tolerant Brevibacillus brevis and arbuscular mycorrhizal fungus can reduce metal acquisition and nickel toxicity effects in plant growing in nickel supplemented soil. Soil Biol Biochem 38:2694–2704

    Article  CAS  Google Scholar 

  • Vivas A, Biró B, Ruiz-Lozano JM, Barea JM, Azcón R (2006c) Two bacterial strains isolated from Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62:1523–1533

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Moreno B, García-Rodriguez S, Benítez E (2009) Assessing the impact of composting and vermicomposting on structural diversity of bacterial communities and enzyme activities of an olive-mill waste. Bioresour Technol 100:1319–1326

    Article  PubMed  CAS  Google Scholar 

  • Vörös I, Biró B, Takács T, Köves-Péchy K, Bujtás K (1998) Effect of arbuscular mycorrhizal fungi on heavy metal toxicity to Trifolium praetense in soils contaminated with Cd, Zn and Ni salts. Agrokém Talaj 47:277–288

    Google Scholar 

  • Weissenhorn I, Leyval C (1995) Root colonization of maize by a Cd-sensitive and a Cd-tolerant Glomus mosseae and cadmium uptake in sand culture. Plant Soil 175:233–237

    Article  CAS  Google Scholar 

  • Weller DM, Thomashow LS (1994) Current challenges in introducing beneficial microorganisms in the rhizosphere. In: O'Gara F, Dowling DN, Boesten B (eds) Molecular ecology of rhizosphere microorganisms: biotechnology and the release of GMOs. VCH Verlagsgesellchaft, Winheim, pp 1–13

    Chapter  Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408. doi:10.1007/s11104-008-9686-1

    Article  CAS  Google Scholar 

  • Whitfield L, Richards AJ, Rimmer DL (2004) Effects of mycorrhizal colonisation on Thymus polytrichus from heavy-metal-contaminated sites in northern England. Mycorrhiza 14:47–54

    Article  PubMed  CAS  Google Scholar 

  • Wöhler I (1997) Auxin-indole derivatives in soils determined by a colorimetric method and by high performance liquid chromatography. Microbiol Res 152:399–405

    Google Scholar 

  • Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR 12–2 that overproduce indoleacetic acid. Curr Microbiol 32:67–71

    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  PubMed  CAS  Google Scholar 

  • Zhou JL (1999) Zn biosorption by Rhizopus arrhizus and other fungi. Appl Microbiol Biotechnol 51:686–693

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosario Azcón .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Ruiz-Lozano, J.M., Azcón, R. (2011). Brevibacillus, Arbuscular Mycorrhizae and Remediation of Metal Toxicity in Agricultural Soils. In: Logan, N., Vos, P. (eds) Endospore-forming Soil Bacteria. Soil Biology, vol 27. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19577-8_12

Download citation

Publish with us

Policies and ethics