Joint immobilization of plant growth-promoting bacteria and green microalgae in alginate beads as an experimental model for studying plant-bacterium interactions

Applied and Environmental Microbiology

Volumn 74, Issue 21, 2008, Pages 6797-6802

  De Bashan, Luz E ^b   Bashan, Yoav ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; PLANT LIFE EXTENSION;

A-PLANT; ALGINATE BEADS; AZOSPIRILLUM; BACTERIAL CONTAMINANTS; EXPERIMENTAL MODELS; EXTERNAL INTERFERENCES; FRESHWATER; MICROALGA; MICROALGAE; PLANT GROWTHS; QUANTITATIVE;

FLOW INTERACTIONS;

ALGINIC ACID; GLUTAMATE DEHYDROGENASE;

ALGINATE; BACTERIUM; EXPERIMENTAL STUDY; GREEN ALGA; INTERSPECIFIC INTERACTION; MICROALGA;

ARTICLE; AZOSPIRILLUM; BACTERIUM CONTAMINATION; CELL INTERACTION; CHLORELLA; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; PHOTOSYNTHESIS; PLANT GROWTH; PROTEIN CONTENT;

ALGINATES; AZOSPIRILLUM; CELLS, IMMOBILIZED; CHLORELLA; GLUCURONIC ACID; HEXURONIC ACIDS; MODELS, THEORETICAL; PLANTS;

AZOSPIRILLUM; BACTERIA (MICROORGANISMS);

EID: 55049083107     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00518-08     Document Type: Article

References (61)

1. Arabidopsis Genome Initiative. 2000. Analysis of the genome of the flowering plant Arabidopsis thaliana. Nature 408:796-815.
2. Arumuganathan, K., and E. D. Earle. 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9:208-218.
3. Barbieri, P., and E. Galli. 1993. Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Res. Microbiol. 144:69-75.
4. Bashan, Y., and L. E. de-Bashan. 2005. Bacteria/plant growth-promotion, p. 103-115. In D. Hillel (ed.), Encyclopedia of soils in the environment, vol. 1. Elsevier, Oxford, United Kingdom.
5. Bashan, Y., G. Holguin, and L. E. de-Bashan. 2004. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can. J. Microbiol. 50:521-577.
6. Bottini, R., F. Cassán, and P. Piccoli. 2004. Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 65:497-503.
7. Burhenne, N., and R. Tischner. 2000. Isolation and characterization of nitrite-reductase-deficient mutants of Chlorella sorokiniana (strain 211-8k). Planta 211:440-445.
8. de-Bashan, L. E., H. Antoun, and Y. Bashan. 2005. Cultivation factors and population size control uptake of nitrogen by the microalgae Chlorella vulgaris when interacting with the microalgae growth-promoting bacterium Azospirillum brasilense. FEMS Microbiol. Ecol. 54:197-203.
9. de-Bashan, L. E., H. Antoun, and Y. Bashan. 2008. Involvement of indole-3-acetic-acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. J. Phycol. 44:938-947.
10. de-Bashan, L. E., Y. Bashan, M. Moreno, V. K. Lebsky, and J. J. Bustillos. 2002. Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. Can. J. Microbiol. 48:514-521.
11. de-Bashan, L. E., J. P. Hernandez, T. Morey, and Y. Bashan. 2004. Microalgae growth-promoting bacteria as "helpers" for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater. Water Res. 38:466-474.
12. de-Bashan, L. E., P. Magallon, H. Antoun, and Y. Bashan. Participation of glutamate dehydrogenase and glutamine synthetase in ammonium assimilation by Chlorella vulgaris jointly immobilized with the microalgae growth-promoting bacterium Azospirillum brasilense. J. Phycol., in press.
13. de-Bashan, L. E., M. Moreno, J. P. Hernandez, and Y. Bashan. 2002. Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris co-immobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense. Water Res. 36:2941-2948.
14. de-Bashan, L. E., A. Trejo, V. A. R. Huss, J. P. Hernandez, and Y. Bashan. 2008. Chlorella sorokiniana UTEX 2805, a heat and intense sunlight tolerant microalgae with potential for removing ammonium from wastewater. Bioresour. Technol. 99:4980-4989.
15. de la Noüe, J., and N. de Pauw. 1988. The potential of microalgal biotechnology: a review of production and uses of microalgae. Biotechnol. Adv. 6:725-770.
16. Devereux, R., A. R. Loeblich III, and G. E. Fox. 1990. Higher plant origins and the phylogeny of green algae. J. Mol. Evol. 31:18-24.
17. Dibb-Fuller, J., and D. A. Morris. 1992. Studies on the evolution of auxin carriers and phytotropin receptors: transmembrane auxin transport in unicellular and multicellular Chlorophyta. Planta 186:219-226.
18. Dobbelaere, S., A. Croonenborghs, A. Thys, A. Vande Broek, and J. Vanderleyden. 1999. Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155-164.
19. Gacesa, P. 1998. Bacterial alginate biosynthesis - recent progress and future prospects. Microbiology 144:1133-1143.
20. Gill, B. S., R. Appels, A. M. Botha-Oberholster, C. R. Buell, J. L. Bennetzen, B. Chalhoub, F. Chumley, J. Dvorák, M. Iwanaga, B. Keller, W. Li, W. R. McCombie, Y. Ogihara, Q. Francis, and S. Takuji. 2004. A workshop report on wheat genome sequencing. Genetics 168:1087-1096.
21. Gonzalez, L. E., and Y. Bashan. 2000. Growth promotion of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant-growth-promoting bacterium Azospirillum brasilense. Appl. Environ. Microbiol. 66:1527-1531.
22. Gonzalez-Bashan, L. E., V. Lebsky, J. P. Hernandez, J. J. Bustillos, and Y. Bashan. 2000. Changes in the metabolism of the microalgae Chlorella vulgaris when co-immobilized in alginate with the nitrogen-fixing Phyllobacterium myrsinacearum. Can. J. Microbiol. 46:653-659.
23. Gopalaswamy, G., S. Kannaiyan, K. J. O'Callaghan, M. R. Davey, and E. C. Cocking. 2000. The xylem of rice (Oryza sativa) is colonized by Azorhizobium caulinodans. Proc. R. Soc. Lond. B 267:103-107.
24. Hartmann, A., M. Singh, and W. Klingmüller. 1983. Isolation and characterization of Azospirillum mutants excreting high amounts of indoleacetic acid. Can. J. Microbiol. 29:916-923.
25. Hartmann, A., and W. Zimmer. 1994. Physiology of Azospirillum, p. 15-39. In Y. Okon (ed.), Azospirillum/ plant associations. CRC Press, Boca Raton, FL.
26. Hernandez, J. P., L. E. de-Bashan, and Y. Bashan. 2006. Starvation enhances phosphorus removal from wastewater by the microalga Chlorella spp. co-immobilized with Azospirillum brasilense. Enzyme Microb. Technol. 38:190-198.
27. Hernandez, J.-P., L. E. de-Bashan, D. J. Rodriguez, Y. Rodriguez, and Y. Bashan. 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., in press.
28. Higashiyama, T., and T. Yamada. 1991. Electrophoretic karyotyping and chromosomal gene mapping of Chlorella. Nucleic Acids Res. 19:6191-6195.
29. Hosono, H., I. Uemura, T. Takumi, T. Nagamune, T. Yasuda, M. Kishimoto, H. Nagashima, N. Shimomura, M. Natori, and I. Endo. 1994. Effect of culture temperature shift on the cellular sugar accumulation of Chlorella vulgaris SO-26. J. Ferment. Bioeng. 78:235-240.
30. Ilangovan, K., R. O. Cañizares-Villanueva, S. González Moreno, and D. Voltolina. 1998. Effect of cadmium and zinc on respiration and photosynthesis in suspended and immobilized cultures of Chlorella vulgaris and Scenedesmus acutus. Bull. Environ. Contam. Toxicol. 60:936-943.
31. International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. Nature 436:793-800.
32. Ishikawa, E., H. Sansawa, and H. Abe. 2004. Isolation and characterization of a Chlorella mutant producing high amounts of chlorophyll and carotenoids. J. Appl. Phycol. 16:385-393.
33. Kennedy, I. R., A. T. M. A. Choudhury, and M. L. Kecskes. 2004. Nonsymbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol. Biochem. 36:1229-1244.
34. Ladha, J. K., and P. M. Reddy (ed.). 2000. The quest for nitrogen fixation in rice. International Rice Research Institute, Los Baños, Laguna, Philippines.
35. Landstein, D., S. Arad, Z. Barak, and D. M. Chipman. 1993. Relationships among the herbicide and functional sites of acetohydroxy acid synthase from Chlorella emersonii. Planta 191:1-6.
36. Lebsky, V. K., L. E. Gonzalez-Bashan, and Y. Bashan. 2001. Ultrastructure of co-immobilization of the microalga Chlorella vulgaris with the plant growth-promoting bacterium Azospirillum brasilense and with its natural associative bacterium Phyllobacterium myrsinacearum in alginate beads. Can. J. Microbiol. 47:1-8.
37. Levanony, H., Y. Bashan, B. Romano, and E. Klein. 1989. Ultrastructural localization and identification of Azospirillum brasilense Cd on and within wheat root by immuno-gold labeling. Plant Soil 117:207-218.
38. Loos, E., and D. Meindl. 1982. Composition of the cell wall of Chlorella fusca. Planta 156:270-273.
39. Malis-Arad, S., M. Friedlander, R. Ben-Arie, and A. E. Richmond. 1980. Alkalinity-induced aggregation in Chlorella vulgaris. I. Changes in cell volume and cell-wall structure. Plant Cell Physiol. 21:27-35.
40. Mazur, A., A. Konop, and R. Synak. 2001. Indole-3-acetic acid in the culture medium of two axenic green microalgae. J. Appl. Phycol. 13:35-42.
41. McHugh, D. J. 2003. A guide to the seaweed industry. FAO Fisheries technical paper no. 441. FAO, Rome, Italy.
42. Northcote, D. H., K. J. Goulding, and R. W. Horne. 1958. The chemical composition and structure of the cell wall of Chlorella pyrenoidosa. Biochem. J. 70:391-397.
43. Oh-Hama, T., and S. Miyachi. 1992. Chlorella, p. 3-26. In M. A. Borowitzka and L. J. Borowitzka (ed.), Microalgal biotechnology. Cambridge University Press, Cambridge, United Kingdom.
44. O'Reilly, A. M., and J. A. Scott. 1995. Defined coimmobilization of mixed microorganism cultures. Enzyme Microb. Technol. 17:636-646.
45. Oswald, W. J. 1992. Microalgae and wastewater treatment, p. 305-328. In M. A. Borowitzka and L. J. Borowitzka (ed.), Microalgal biotechnology. Cambridge University Press, Cambridge, United Kingdom.
46. Perrine, F. M., J. Prayitno, J. J. Weinman, F. B. Dazzo, and B. G. Rolfe. 2001. Rhizobium plasmids are involved in the inhibition or stimulation of rice growth and development. Aust. J. Plant Physiol. 28:923-937.
47. Piro, G., M. Lenucci, G. Dalessandro, N. La Rocca, N. Rascio, I. Moro, and C. Andreoli. 2000. Ultrastructure, chemical composition and biosynthesis of the cell wall in Koliella antarctica (Klebsormidiales, Chlorophyta). Eur. J. Phycol. 35:331-337.
48. Puente, M. E., Y. Bashan, C. Y. Li, and V. K. Lebsky. 2004. Microbial populations and activities in the rhizoplane of rock-weathering desert plants. I. Root colonization and weathering of igneous rocks. Plant Biol. 6:629-642.
49. Ramazanov, A., and Z. Ramazanov. 2006. Isolation and characterization of a starchless mutant of Chlorella pyrenoidosa STL-PI with a high growth rate, and high protein and polyunsaturated fatty acid content. Phycol. Res. 54:255-259.
50. Ramos, H. J. O., L. D. B. Roncato-Maccari, E. M. Souza, J. R. L. Soares-Ramos, M. Hungria, and F. O. Pedrosa. 2002. Monitoring Azospirillumwheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J. Biotechnol. 97:243-252.
51. Raven, P. H., R. H. Evert, and S. E. Eichhorn. 1992. Biology of plants, 5th ed. Worth Publishers, New York, NY.
52. Richmond, A. 1990. Handbook of microalgal mass culture. CRC Press, Boca Raton, FL.
53. Romo, S., and C. Perez-Martinez. 1997. The use of immobilization in alginate beads for long-term storage of Pseudoanabaena galeata (Cyanobacteria) in the laboratory. J. Phycol. 33:1073-1076.
54. Smidsrød, O., and G. Skjak-Braek. 1990. Alginate as immobilization matrix for cells. Trends Biotechnol. 8:71-78.
55. Spaepen, S., J. Vanderleyden, and R. Remans. 2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31:425-448.
56. Steenhoudt, O., and J. Vanderleyden. 2000. Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev. 24:487-506.
57. Stirk, W. A., V. Ordog, J. Van Staden, and K. Jager. 2002. Cytokinin-and auxin-like activity in cyanophyta and microalgae. J. Appl. Phycol. 14:215-221.
58. Tam, N. F. Y., and Y. S. Wong. 2000. Effect of immobilized microalgal bead concentration on wastewater nutrient removal. Environ. Pollut. 107:145-151.
59. Vande Broek, A., M. Lambrecht, K. Eggermont, and J. Vanderleyden. 1999. Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J. Bacteriol. 181:1338-1342.
60. Yabur, R., Y. Bashan, and G. Hernández-Carmona. 2007. Alginate from the macroalgae Sargassum sinicola as a novel source for microbial immobilization material in wastewater treatment and plant growth promotion. J. Appl. Phycol. 19:43-53.
61. Yanni, Y. G., R. Y. Rizk, F. K. Abd El-Fattah, A. Squartini, V. Corich, A. Giacomini, F. deBruijn, J. Rademaker, J. Maya-Flores, P. Ostrom, M. Vega-Hernandez, R. I. Hollingsworth, E. Martinez-Molina, P. Mateos, E. Velazquez, J. Wopereis, E. Triplett, M. Umali-Garcia, J. A. Anarna, B. G. Rolfe, J. K. Ladha, J. Hill, R. Mujoo, P. K. Ng, and F. B. Dazzo. 2001. The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust. J. Plant Physiol. 28:845-870.