Bacillus pumilus ES4: Candidate plant growth-promoting bacterium to enhance establishment of plants in mine tailings

Environmental and Experimental Botany

Volumn 69, Issue 3, 2010, Pages 343-352

  de Bashan, Luz E ^a,b   Hernandez, Juan Pablo ^b   Bashan, Yoav ^a,b   Maier, Raina M ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

Author keywords

Bacillus; DGGE; FISH; Mine tailings; Phytostabilization

Indexed keywords

BACTERIUM; DICOTYLEDON; ELECTROKINESIS; EXPERIMENTAL STUDY; GROWTH RATE; MICROBIAL COMMUNITY; MINE WASTE; POLYMERASE CHAIN REACTION; ROOT COLONIZATION; ROOT-SHOOT RATIO; TAILINGS;

ATRIPLEX; ATRIPLEX LENTIFORMIS; AZOSPIRILLUM BRASILENSE; BACILLUS (BACTERIUM); BACILLUS PUMILUS; BACTERIA (MICROORGANISMS);

EID: 77954033035     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2010.04.014     Document Type: Article

References (74)

1. Amman R.I., Binder B.J., Olson R.J., Chisholm S.W., Devereux R., Stahl D.A. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 1990, 56:1919-1925.
2. Arsene F., Katupitiya S., Kennedy I.R., Elmerich C. Use of LacZ fusions to study the expression of nif genes of Azospirillum brasilense in association with plants. Mol. Plant: Microbe Int. 1994, 7:748-757.
3. Assmus B., Hutzler P., Kirchhof G., Amann R., Lawrence J.R., Hartmann A. In situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl. Environ. Microbiol. 1995, 61:1013-1019.
4. Bacilio M., Rodriguez H., Moreno M., Hernandez J.-P., Bashan Y. Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biol. Fertil. Soils 2004, 40:188-193.
5. Bashan Y. Significance of timing and level of inoculation with rhizosphere bacteria on wheat plants. Soil Biol. Biochem. 1986, 18:297-301.
6. Bashan Y. Alginate beads as synthetic inoculant carriers for the slow release of bacteria that affect plant growth. Appl. Environ. Microbiol. 1986, 51:1089-1098.
7. Bashan Y., de-Bashan L.E. Bacteria/plant growth-promotion. Encyclopedia of Soils in the Environment 2005, vol. 1:103-115. Elsevier, Oxford, U.K.
8. Bashan Y., de-Bashan L.E. Fresh-weight measurements of roots provide inaccurate estimates of the effects of plant growth-promoting bacteria on root growth: a critical examination. Soil Biol. Biochem. 2005, 37:1795-1804.
9. Bashan Y., Dubrovsky J.G. Azospirillum spp. participation in dry matter partitioning in grasses at the whole plant level. Biol. Fertil. Soils 1996, 23:435-440.
10. Bashan Y., Hernandez J.-P., Leyva L.A., Bacilio M. Alginate microbeads as inoculant carrier for plant growth-promoting bacteria. Biol. Fertil. Soils 2002, 35:359-368.
11. Bashan Y., Holguin G. Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol. Biochem. 1998, 30:1225-1228.
12. Bashan Y., Holguin G., de-Bashan L.E. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can. J. Microbiol. 2004, 50:521-577.
13. Bashan Y., Levanony H. Alterations in membrane potential and in proton efflux in plant roots induced by Azospirillum brasilense. Plant Soil 1991, 137:99-103.
14. Bashan Y., Moreno M., Troyo E. Growth promotion of the oilseed halophyte Salicornia bigelovii in seawater inoculated with mangrove rhizosphere bacteria and Azospirillum. Biol. Fertil. Soils 2000, 32:265-272.
15. Bashan Y., Salazar B., Puente M.E. Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house. Biol. Fertil. Soils 2009, 45:655-662.
16. Bashan Y., Salazar B., Puente M.E., Bacilio M., Linderman R.G. Enhanced establishment and growth of giant cardon cactus in an eroded field in the Sonoran Desert using native legume trees as nurse plants aided by plant growth-promoting microorganisms and compost. Biol. Fertil. Soils 2009, 45:585-594.
17. Belimov A.A., Kunakova A.M., Safronova V.I., Stepanok V.V., Yudkin L.V., Alekseev Y.V., Kozhemyakov A.P. Employment of rhizobacteria for the inoculation of barley plants cultivated in soil contaminated with lead and cadmium. Microbiology 2004, 73:99-106.
18. Burd G.I., Dixon D.G., Glick B.R. A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol. 1998, 64:3663-3668.
19. Burd G.I., Dixon D.G., Glick B.R. Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can. J. Microbiol. 2000, 46:237-245.
20. Carrillo A.E., Li C.Y., Bashan Y. Increased acidification in the rhizosphere of cactus seedlings induced by Azospirillum brasilense. Naturwissenschaften 2002, 89:428-432.
21. Chiu K.K., Ye Z.H., Wong M.H. Growth of Vetiveria zizanioides and Phragmities australis on Pb/Zn and Cu mine tailings amended with manure compost and sewage sludge: a greenhouse study. Bioresour. Technol. 2006, 97:158-170.
22. Colores G.M., Macur R.E., Ward D.M., Inskeep W.P. Molecular analysis of surfactant-driven microbial population shifts in hydrocarbon-contaminated soil. Appl. Environ. Microbiol. 2000, 66:2959-2964.
23. Daims H., Stoecker K., Wagner M. Fluorescence in situ hybridization for the detection of prokaryotes. Molecular Microbial Ecology 2005, Taylor and Francis Group, New York. A.M. Osborn, C.J. Smith (Eds.).
24. de Brito-Alvarez M.A., Gagne S., Antoun H. Effect of compost on rhizosphere microflora of the tomato and on the incidence of plant growth-promoting rhizobacteria. Appl. Environ. Microbiol. 1995, 61:194-199.
25. EPA, 2004. Test Methods for Evaluating Solid Waste. EPA SW-846, US Environmental Protection Agency. Washington, DC.
26. Enebak S.A., Wei G., Kloepper J.W. Effects of plant growth-promoting rhizobacteria on loblolly and slash pine seedlings. For. Sci. 1998, 44:139-144.
27. Felici C., Vettori L., Giraldi E., Forino L.M.C., Toffanon A., Tagliasacchi A.M., Nuti M. Single and co-inoculation of Bacillus subtilis and Azospirillum brasilense on Lycopersicon esculentum: Effects on plant growth and rhizosphere microbial community. Appl. Soil Ecol. 2008, 40:260-270.
28. Felske A., Akkermans A.D.L., de Vos W.M. Quantification of 16S rRNA in complex bacterial communities by multiple competitive reverse transcription-PCR in temperate gradient gel electrophoresis fingerprintings. Appl. Environ. Microbiol. 1998, 64:4581-4587.
29. Ferris M.J., Muyzer G., Ward D.M. Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl. Environ. Microbiol. 1996, 62:340-346.
30. Glick B.R. Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol. Adv. 2003, 21:383-393.
31. Gonzalez-Chavez M.C., Carrillo-Gonzalez R., Gutierrez-Castorena M.C. Natural attenuation in a slag heap contaminated with cadmium: The role of plants and arbuscular mycorrhizal fungi. J. Hazard Mater. 2009, 161:1288-1298.
32. Grandlic C.J., Mendez M.O., Chorover J., Machado B., Maier R.M. Plant growth-promoting bacteria for phytostabilization of mine tailings. Environ. Sci. Technol. 2008, 42:2079-2084.
33. Grandlic C.J., Palmer M.W., Maier R.M. Optimization of plant growth-promoting bacteria-assisted phytostablization of mine tailings. Soil Biol. Biochem. 2009, 41:1734-1740.
34. Hartmann A., Rothballer M., Schmid M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 2008, 312:7-14.
35. Hernandez J.-P., de-Bashan L.E., Rodriguez D.J., Rodriguez Y., Bashan Y. Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils. Eur. J. Soil Biol. 2009, 45:88-93.
36. Herschkovitz Y., Lerner A., Davidov Y., Okon Y., Jurkevitch E. Azospirillum brasilense does not affect population structure of specific rhizobacterial communities of inoculated maize (Zea mays). Environ. Microbiol. 2005, 7:1847-1852.
37. Herschkovitz Y., Lerner A., Davidov Y., Rothballer M., Hartmann A., Okon Y., Jurkevitch E. Inoculation with the plant growth promoting rhizobacterium Azospirillum brasilense causes little disturbance in the rhizosphere and rhizoplane of maize (Zea mays). Microbial Ecol 2005, 50:277-288.
38. Iverson S.L., Maier R.M. Effects of compost on colonization of roots of plants grown in metalliferous mine tailings, as examined by fluorescence in situ hybridization. Appl. Environ. Microbiol. 2009, 75:842-847.
39. Jacoud C., Faure D., Wadoux P., Bally R. Development of a strain-specific probe to follow inoculated Azospirillum lipoferum CRT1 under field conditions and enhancement of maize root development by inoculation. FEMS Microbiol. Ecol. 1998, 27:43-51.
40. Kirchhof G., Schloter M., Assmus B., Hartmann A. Molecular microbial ecology approaches applied to diazotrophs associated with non-legumes. Soil Biol. Biochem. 1997, 29:853-862.
41. Kloepper J.W., Reddy M.S., Rodríguez-Kabana R., Kenney D.S., Kokalis-Burelle N., Martinez-Ochoa N., Vavrina C.S. Application for rhizobacteria in transplant production and yield enhancement. Acta Horticulturae 2004, 631:217-229.
42. Kloepper J.W., Ryu C.-M., Zhang S. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 2004, 94:1259-1266.
43. Lerner A., Herschkovitz Y., Baudoin E., Nazaret S., Moenne-Loccoz Y., Okon Y., Jurkevitch E. Effect of Azospirillum brasilense inoculation on rhizobacterial communities analyzed by denaturing gradient gel electrophoresis and automated ribosomal intergenic spacer analysis. Soil Biol. Biochem. 2006, 38:1212-1218.
44. Li W.C., Ye Z.H., Wong M.H. Effects of bacteria on enhanced metal uptake of the Cd/Zn-hyperaccumulating plant, Sedum alfredii. J. Exper. Bot. 2007, 58:4173-4182.
45. Liu W.-T., Mirzaberok A.D., Stahl D.A. Optimization of an oligonucleotide microchip for microbial identification studies: a non-equilibrium dissociation approach. Environ. Microbiol. 2001, 3:619-629.
46. Lugtenberg B.J.J., Dekkers L.C. What makes Pseudomonas bacteria rhizosphere competent?. Environ. Microbiol. 1999, 1:9-13.
47. McCutcheon S.C., Schnoor J.L. Phytoremediation: Transformation and Control of Contaminants 2003, Wiley-Interscience, Hoboken, NJ.
48. Mendez M.O., Glenn E.P., Maier R.M. Phytostabilization potential of quailbush for mine tailings: Growth, metal accumulation, and microbial community changes. J Environ. Qual. 2007, 36:245-253.
49. Mendez M.O., Maier R.M. Phytostabilization of mine tailings in arid and semiarid environments-an emerging remediation technology. Environ. Health Perspect. 2008, 116:278-283.
50. Meyer J.R., Linderman R.G. Selective influence on populations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed by Glomus fasciculatum. Soil Biol. Biochem. 1986, 18:191-196.
51. Mogge B., Loferer C., Agerer R., Hutzler P., Hartmann A. Bacterial community structure and colonization patterns of Fagus sylvatica L. ectomycorrhizospheres as determined by fluorescence in situ hybridization and confocal laser scanning microscopy. Mycorrhiza 2000, 9:271-278.
52. Natarajan K.A. An integrated biotechnological approach to gold processing-an Indian experience. Miner. Process. Extr. Metall. Rev. 1998, 19:235-251.
53. Petrisor I., Dobrota S., Komnitsas K., Lazar I., Kuperberg J.M., Serban M. Artificial inoculation-perspectives in tailings phytostabilization. Int. J. Phytorem. 2004, 6:1-15.
54. Pilon-Smits E. Phytoremediation. Annu. Rev. Plant Biol. 2005, 56:15-39.
55. Pishchik V.N., Vorobyev N.I., Chernyaeva I.I., Timofeeva S.V., Kozhemyakov A.P., Alexeev Y.V., Lukin S.M. Experimental and mathematical simulation of plant growth promoting rhizobacteria and plant interaction under cadmium stress. Plant Soil. 2002, 243:173-186.
56. Puente M.E., Bashan Y., Li C.Y., Lebsky V.K. Microbial populations and activities in the rhizoplane of rock-weathering desert plants. I. Root colonization and weathering of igneous rocks. Plant Biol. 2004, 6:629-642.
57. Ramos H.J.O., Roncato-Maccari L.D.B., Souza E.M., Soares-Ramos J.R.L., Hungria M., Pedrosa F.O. Monitoring Azospirillum-wheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J. Biotechnol. 2002, 97:243-252.
58. Reed M.L.E., Glick B.R. Growth of canola (Brassica napus) in the presence of plant growth-promoting bacteria and either copper or polycyclic aromatic hydrocarbons. Can. J. Microbiol. 2005, 51:1061-1069.
59. Reed M.L.E., Warner B.G., Glick B.R. Plant growth-promoting bacteria facilitate the growth of the common reed Phragmites australis in the presence of copper or polycyclic aromatic hydrocarbons. Curr. Microbiol. 2005, 51:425-429.
60. Rajkumar M., Freitas H. Effects of inoculation of plant growth-promoting bacteria on Ni uptake by Indian mustard. Bioresour. Technol. 2008, 99:3491-3498.
61. Rajkumar M., Freitas H. Influence of metal-resistant plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 2008, 71:834-842.
62. Rosario K., Iverson S.L., Henderson D.A., Chartrand S., McKeon C., Glenn E.P., Maier R.M. Bacterial community changes during plant establishment at the San Pedro River mine tailings site. J. Environ. Qual. 2007, 3:1249-1259.
63. Ryu C.-M., Hu C.-H., Locy R.D., Kloepper J.W. Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 2005, 268:285-292.
64. Laboratory Methods Manual, 2004. In: Burt, R. (Ed.), Soil Survey Laboratory Investigations Report No. 42, Version 4.0. National Resources Conservation Service, Lincoln, NE.
65. Tsuruta T. Removal and recovery of uranium using microorganisms isolated from North American uranium deposits. Am. J. Environ. Sci. 2007, 3:60-66.
66. Venables W.N., Ripley B.D. Modern Applied Statistics with S 2002, Springer, New York, pp. 385-389. 4th ed.
67. Vessey J.K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil. 2003, 255:571-586.
68. Vijayalakshmi S.P., Raichur A.M. The utility of Bacillus subtilis as a bioflocculant for fine coal. Colloids Surf. B: Biointerfaces 2003, 29:265-275.
69. Vivas A., Biro B., Ruiz-Lozano J.M., Barea J.M., Azcon R. Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 2006, 62:1523-1533.
70. Wu S.C., Cheung K.C., Luo Y.M., Wong H.M. Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ. Pollut. 2006, 140:124-135.
71. Wu S.C., Luo Y.M., Cheung K.C., Wong M.H. Influence of bacteria on Pb and Zn speciation, mobility and bioavailability in soil: a laboratory study. Environ. Pollut. 2006, 144:765-773.
72. Ye Z.H., Yang Z.Y., Chan G.Y.S., Wong M.H. Growth response of Sesbania rostrata and S. cannabina to sludge-amended lead/zinc mine tailings. A greenhouse study. Environ. Int. 2001, 26:449-455.
73. Zhang H.-B., Yang M.-X., Shi W., Zheng Y., Sha T., Zhao Z.-W. Bacterial diversity in mine tailings compared by cultivation and cultivation-independent methods and their resistance to lead and cadmium. Microb. Ecol. 2007, 54:705-712.
74. Zhuang X., Chen J., Shim H., Bai Z. New advances in plant growth-promoting rhizobacteria for bioremediation. Environ. Int. 2007, 33:406-413.