Abstract
Chromium (Cr), with its great economic importance in industrial use, is a major metal pollutant of the environment. It affects soil microbial activity and soil fertility, resulting in losses in yield of plants. Paenibacillus lentimorbus B-30488r (B-30488r) tolerated 200 μg ml−1 of Cr under in vitro conditions and produced the plant growth promoting substance indole acetic acid in the presence of Cr. Our in vitro study indicates enhancement in B-30488r biofilm formation by sodium alginate (SA) and calcium chloride (CaCl2) both in absence and presence of supplemented Cr(VI) as compared to unsupplemented control. The plant growth promoting effects caused by the B-30488r biofilm in rhizosphere of chickpea under Cr(VI) stress suggests a phytoprotective role of B-30488r biofilm. Our study reflects the multifarious role of strain B-30488r and presents it as a potent plant growth promoting and bioremediation agent useful in Cr-contaminated rhizosphere soil, whereby the SA and CaCl2 induced B-30488r biofilm on plant root acts as a shield in preventing the direct access of toxic Cr to plant tissues, thus reducing its uptake in plants.
References
Abdul Baki A, Anderson JD (1973) Vigour determination in soyabean seed by multiple criterion. Crop Sci 13:630–633
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Cassidy MB, Lee H, Trevors JT (1996) Environmental applications of immobilized microbial cells: a review. J Ind Microbiol 16:17–101
Cervantes C, Campos-Garcia J, Devars S, Gutierrez-Corona F, Loza-Tavera H, Torres-Guzman JC, Moreno-Sanchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347
Chatterjee S, Sau GB, Mukherjee SK (2009) Plant growth promotion by a hexavalent chromium reducing bacterial strain, Cellulosimicrobium cellulans KUCr3. World J Microbiol Biotechnol 25:1829–1836
Clijsters H, Van Assche F (1985) Inhibition of photosynthesis by heavy metals. Photosynth Res 7:31–40
Coleman RN, Paran JH (1991) Biofilm concentration of chromium. Environ Technol 12:1079–1093
Costerton JW, Irvin RT, Cheng KJ (1981) The bacterial glycocalyx in nature and disease. Annu Rev Microbiol 35:299–324
DasGupta SM, Khan N, Nautiyal CS (2006) Biologic control ability of plant growth-promoting Paenibacillus lentimorbus NRRL B-30488 isolated from milk. Curr Microbiol 53:502–505
Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867
Dhal B, Thatoi H, Das N, Pandey BD (2010) Reduction of hexavalent chromium by Bacillus sp. isolated from chromite mine soils and characterization of reduced product. J Chem Technol Biotechnol 85:1471–1479
Fenice M, Selbman L, Federici F, Vassilev N (2000) Application of encapsulated Penicillium variabile P16 in solubilization of rock phosphate. Bioresour Technol 73:157–162
Harrison JJ, Ceri H, Turner RJ (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5:928–938
Hegazi GAE (2011) Viability of encapsulated shoot tips of Capparis orientalis Duh. Nat Sci 9(8):223–228
Kathiravan MN, Karthick R, Muthu N, Muthukumar K, Velan M (2010) Sonoassisted microbial reduction of chromium. Appl Biochem Biotechnol 160:2000–2013
Khan N, Mishra A, Chauhan PS, Nautiyal CS (2011) Induction of Paenibacillus lentimorbus biofilm by sodium alginate and CaCl2 alleviates drought stress in chickpea. Ann Appl Biol (in press)
Langley S, Beveridge TJ (1999) Metal binding by Pseudomonas aeruginosa PAO1 is influenced by growth of the cells as a biofilm. Can J Microbiol 45:616–622
Ledin M (2000) Accumulation of metals by microorganisms—processes and importance for soil systems. Earth-Sci Rev 51:1–31
Lloyd JR, Lovley DR (2001) Microbial detoxification of metals and radionuclides. Curr Opin Biotechnol 12:248–253
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin Phenol Reagent. J Biol Chem 193:265–275
Molina MA, Ramos JL, Espinosa-Urgel M (2003) Plant-associated biofilms. Rev Environ Sci Biotechnol 2:99–108
Nautiyal CS (1997) Rhizosphere competence of Pseudomonas sp. NBRI9926 and Rhizobium sp. NBRI9513 involved in the suppression of chickpea (Cicer arietinum L.) pathogenic fungi. FEMS Microbiol Ecol 23:145–158
Nautiyal CS, Mehta SD, Singh HB, Pushpangadan P (2006) Synergistic bioinoculant composition comprising bacterial strains of accession nos. NRRL B-30486, NRRL B-30487 and NRRL B-30488 and method of producing said composition thereof. U.S. Patent 7097830
Niu C, Gilbert ES (2004) Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl Environ Microbiol 70:6951–6956
Paul E, Fages J, Blanc P, Goma G, Pareilleux A (1993) Survival of alginate-entrapped cells of Azospirillum lipoferum during dehydration and storage in relation to water properties. Appl Microbiol Biotechnol 40:34–39
Priester JH, Olson SG, Webb SM, Neu MP, Hersman LE, Holden PA (2006) Enhanced exopolymer production and chromium stabilization in Pseudomonas putida unsaturated biofilms. Appl Environ Microbiol 72(3):1988–1996
Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748
Ramírez-Díaz MI, Díaz-P′erez C, Vargas E, Riveros-Rojas H, Campos-García J, Cervantes C (2008) Mechanisms of bacterial resistance to chromium compounds. Biometals 21:321–332
Schons PF, Lopes FC, Battestin V, Macedo GA (2011) Immobilization of Paecilomyces variotii tannase and properties of the immobilized enzyme. J Microencapsul 28(3):211–219
Seneviratne G, Zavahir JS, Bandara WMMS, Weerasekara MLMAW (2007) Fungal-bacterial biofilms: their development for novel biotechnological applications. World J Microbiol Biotechnol 24(6):739–743
Shanker AK, Djanaguiraman M, Sudhagar R, Chandrashekar CN, Pathmanabhan G (2004) Differential antioxidative response of ascorbate glutathione pathway enzymes and metabolites to chromium speciation stress in green gram (Vigna radiata (L.) R.Wilczek. cv CO4) roots. Plant Sci 166:1035–1043
Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397
Smidsrød O, Skjak-Braek G (1990) Alginate as immobilization matrix for cells. Trends Biotechnol 8:71–78
Srivastava S, Yadav A, Seem K, Mishra S, Chaudhary V, Nautiyal CS (2008) Effect of high temperature on Pseudomonas putida NBRI0987 biofilm formation and expression of stress sigma factor RpoS. Curr Microbiol 56:453–457
Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69:2313–2320
Walker HL, Connick WJ Jr (1983) Sodium alginate for production and formulation of mycoherbicides. Weed Sci 31:333–338
Wang YT (2000) Microbial reduction of chromate. In: Lovely DR (ed) Environmental microbe-metal interactions. American Society for Microbiology, Washington, pp 225–235
Wani PA, Khan S, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163
Wolfaardt GM, Lawrence JR, Headley JV, Robarts RD, Caldwell DE (1994) Microbial exopolymers provide a mechanism for bioaccumulation of contaminants. Microb Ecol 27:279–291
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. J Biochem 57:508–554
Acknowledgments
The study was supported by Task force grant NWP-006 from Council of Scientific and Industrial Research (CSIR), New Delhi, India. NK thanks CSIR for awarding Senior Research Fellowship.
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Khan, N., Mishra, A., Chauhan, P.S. et al. Paenibacillus lentimorbus enhances growth of chickpea (Cicer arietinum L.) in chromium-amended soil. Antonie van Leeuwenhoek 101, 453–459 (2012). https://doi.org/10.1007/s10482-011-9637-3
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DOI: https://doi.org/10.1007/s10482-011-9637-3