Development of alginate-based aggregate inoculants of Methylobacterium sp. and Azospirillum brasilense tested under in vitro conditions to promote plant growth

Journal of Applied Microbiology

Volumn 116, Issue 2, 2014, Pages 408-423

  Joe, M M ^a,b   Saravanan, V S ^c   Islam, M R ^d   Sa, T ^a  

^a Chungbuk National University   (South Korea)

^b VELS INSTITUTE OF SCIENCE   (India)

^c Pondicherry University   (India)

^d Inha University   (South Korea)

Author keywords

ACC deaminase; Azospirillum brasilense; Biofilm; Co aggregation; Methylobacterium oryzae; Plant growth promoting bacteria; Water stress

Indexed keywords

AGGLOMERATION; ALGINATE; BACTERIA; EFFICIENCY; FRUITS;

ACC DEAMINASE; AZOSPIRILLUM BRASILENSE; BACTERIAL INOCULANTS; CO-AGGREGATION; CONDITION; METHYLOBACTERIA ORYZA; METHYLOBACTERIUM; PLANT GROWTH PROMOTING BACTERIUM; PLANT GROWTH PROMOTION; WATER STRESS;

BIOFILMS;

ALGINIC ACID; ESTERASE; GLUCAN SYNTHASE; METHYLCELLULOSE; NANOBEAD; PECTIN; PECTIN LYASE; PEROXIDASE; ETHYLENE; ETHYLENE DERIVATIVE; GLUCURONIC ACID; HEXURONIC ACID; MALONALDEHYDE; MICROSPHERE; SOIL;

AGGREGATION; ALGINATE; BACTERIUM; BIOFILM; FRUIT; SURVIVAL; WATER STRESS;

AGRICULTURAL INOCULATION; ARTICLE; AZOSPIRILLUM BRASILENSE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BIOFILM; COCULTURE; CONTROLLED STUDY; DROUGHT; DRY WEIGHT; ENZYME ACTIVITY; IN VITRO STUDY; LIPID PEROXIDATION; METHYLOBACTERIUM; METHYLOBACTERIUM ORYZAE; METHYLOBACTERIUM SUOMIENSE; MICROBIAL POPULATION DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GROWTH; PLANT STRESS; SCANNING ELECTRON MICROSCOPE; SHELF LIFE; SOIL MOISTURE; TOMATO; WATER STRESS; CHEMISTRY; DEHYDRATION; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HYDROLYSIS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; SOIL; ULTRASTRUCTURE;

AZOSPIRILLUM BRASILENSE; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; METHYLOBACTERIUM; METHYLOBACTERIUM SP.; METHYLOBACTERIUM SUOMIENSE;

ALGINATES; AZOSPIRILLUM BRASILENSE; BIOFILMS; DEHYDRATION; DROUGHTS; ETHYLENES; GLUCURONIC ACID; HEXURONIC ACIDS; HYDROLYSIS; LIPID PEROXIDATION; LYCOPERSICON ESCULENTUM; MALONDIALDEHYDE; METHYLOBACTERIUM; MICROSCOPY, ELECTRON, SCANNING; MICROSPHERES; PEROXIDASE; SOIL;

EID: 84892491841     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12384     Document Type: Article

References (62)

1. Albersheim, P. (1966) Pectin lyase from fungi. Methods Enzymol 8, 628-631.
2. del Amor, F.M. and Cuadra-Crespo, P. (2011) Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct Plant Biol 39, 82-90.
3. Arunika, H.L., Gunawardena, A.N., Greenwood, J.S. and Dengler, N.G. (2007) Cell wall degradation and modification during programmed cell death in lace plant, Aponogeton madagascariensis (Aponogetonaceae). Am J Bot 94, 1116-1128.
4. Bashan, Y. (1986a) Significance of timing and level of inoculation with rhizosphere bacteria on wheat plants. Soil Biol Biochem 18, 297-301.
5. Bashan, Y. (1986b) Alginate beads as synthetic inoculant carriers for the slow release of bacteria that affect plant growth. Appl Environ Microbiol 51, 1089-1098.
6. Bashan, Y. and de-Bashan, L.E. (2010) How the plant growth-promoting bacterium A. brasilense promotes plant growth-a critical assessment. Adv Agron 108, 77-136.
7. Bashan, Y. and Gonzalez, L.E. (1999) Long-term survival of the plant-growth-promoting bacteria Azospirillum brasilense and Pseudomonas fluorescens in dry alginate inoculant. Appl Microbiol Biotechnol 51, 262-266.
8. Bashan, Y. and Holguin, G. (1993) Anchoring of Azospirillum brasilense to hydrophobic polystyrene and wheat roots. J Gen Microbiol 139, 379-385.
9. Bashan, Y. and Holguin, G. (1997) Azospirillum-plant relationships: environmental and physiological advances (1990-1996). Can J Microbiol 43, 103-121.
10. Bashan, Y. and Levanony, H. (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36, 591-608.
11. Bashan, Y., Mitiku, G., Whitmoyer, R.E. and Levanony, H. (1991) Evidence that fibrillar anchoring is essential for Azospirillum brasilense Cd attachment to sand. Plant Soil 132, 73-83.
12. Bashan, Y., Hernandez, J.P., Leyva, L.A. and Bacilio, M. (2002) Alginate microbeads as inoculant carrier for plant growth-promoting bacteria. Biol Fert Soils 35, 359-368.
13. de-Bashan, L.E., Schmid, M., Rothballer, M., Hartmann, A. and Bashan, Y. (2011) Cell-cell interaction in the eukaryote-prokaryote model using the microalgae Chlorella vulgaris and the bacterium Azospirillum brasilense immobilized in polymer beads. J Phycol 47, 1350-1359.
14. Black, C.A. (1965) Methods of Soil Analysis: Part I Physical and Mineralogical Properties. Madison, WI: American Society of Agronomy.
15. Blaha, D., Prigent-Combaret, C., Mirza, M.S. and Moenne-Loccoz, Y. (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56, 455-470.
16. Burdman, S., Jurkevitch, E., Schwartsburd, B., Hampel, M. and Okon, Y. (1998) Aggregation in A. brasilense: effects of chemical and physical factors and involvement of extracellular components. Microbiology 144, 1989-1999.
17. Burdman, S., Jurketvitch, E., Soria-Diaz, M.E., Gil Serrano, A.M. and Okon, Y. (2000) Extracellular polysaccharide composition of Azospirillum brasilense and its relation with cell aggregation. FEMS Microbiol Lett 489, 259-264.
18. Cisar, J.O., Kolenbrander, P.E. and McIntire, F.C. (1979) Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun 24, 742-752.
19. Corpe, W.A. and Basil, D.V. (1982) Methanol-utilizing bacteria, associated with green plants. Dev Indust Microbiol 23, 483-493.
20. Creus, C.M., Sueldo, R.J. and Barassi, C.A. (1997) Shoot growth and water status in Azospirillum-inoculated wheat seedlings grown under osmotic and salt stresses. Plant Physiol Biochem 35, 939-944.
21. Del Re, B., Sgorbati, B., Miglioli, M. and Palenzona, D. (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31, 438-442.
22. Djordjevic, D., Wiedmann, M. and McLandsborough, L.A. (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68, 2950-2958.
23. Duan, X., Liu, T., Zhang, D., Su, X., Lin, H. and Jiang, Y. (2011) Effect of pure oxygen atmosphere on antioxidant enzyme and antioxidant activity of harvested litchi fruit during storage. Food Res Int 44, 1905-1911.
24. El-Komy, H.M., Hamdia, M.A. and Abd El-Baki, G.K. (2003) Nitrate reductase in wheat plants grown under water stress and inoculated with Azospirillum spp. Biol Plantarum 46, 281-287.
25. Esquivel-Cote, R., Ramírez-Gama, R.M., Tsuzuki-Reyes, G., Orozco-Segovia, A. and Huante, P. (2010) A. brasilense lipoferum strain AZm5 containing 1-aminocyclopropane-1-carboxylic acid deaminase improves early growth of tomato seedlings under nitrogen deficiency. Plant Soil 337, 65-75.
26. Felici, C., Vettori, L., Giraldi, E., Forino, L.M.C., Toffanin, A., Tagliasacchi, A.M. and Nuti, M. (2008) Single and co-inoculation of Bacillus subtilis and Azospirillum brasilense on Lycopersicon esculentum: effects on plant growth and rhizosphere microbial community. Appl Soil Ecol 40, 260-270.
27. Gaspar, T., Penel, C., Thorpe, T. and Greppin, H. (1982) Peroxidases: A Survey of their Biochemical and Physiological Roles in Higher Plants. Geneva: University of Geneva Press.
28. Glick, B.R., Penrose, D.M. and Li, J. (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190, 63-68.
29. Hagerman, A.E. and Austin, P.J. (1986) Continuous spectrophotometric assay for plant pectin methyl esterase. J Agric Food Chem 34, 440-444.
30. Halsall, D.M. and Goodchild, D.J. (1986) Nitrogen fixation associated with development and localization of mixed populations of Cellulomonas sp. and A. brasilense grown on cellulose or wheat straw. Appl Environ Microbiol 51, 849-854.
31. Handley, P.S., Harty, D.W., Wyatt, J.E., Brown, C.R., Doran, J.P. and Gibbs, A.C. (1987) A comparison of the adhesion, coaggregation and cell-surface hydrophobicity properties of fibrillar and fimbriate strains of Streptococcus salivarius. J Gen Microbiol 133, 3207-3217.
32. Hartmann, A. and Bashan, Y. (2009) Ecology and application of Azospirillum and other plant growth-promoting bacteria (PGPB)-Special Issue. Eur J Soil Biol 45, 1-2.
33. Idris, R., Trifonova, R., Puschenreiter, M., Wenzel, W.W. and Sessitsch, A. (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70, 2667-2677.
34. Joe, M.M., Karthikeyan, B., Chauhan, P.S., Shagol, C., Islam, R., Deiveekasundaram, M. and Sa, T. (2012) Survival of Azospirillum brasilense flocculated cells in alginate and its inoculation effect on growth and yield of maize under water deficit conditions. Eur J Soil Boil 50, 198-206.
35. Joe, M.M., Saravanan, V.S. and Sa, T. (2013) Aggregation of selected plant growth promoting Methylobacterium strains: role of cell surface components and hydrophobicity. Arch Microbiol 195, 219-225.
36. Khammas, K.M. and Kaiser, P. (1992) Pectin decomposition and associated nitrogen fixation by mixed cultures of Azospirillum brasilense and Bacillus species. Can J Microbiol 38, 794-797.
37. Kim, C., Kecskés, M.L., Deaker, R.J., Gilchrist, K., New, P.B., Kennedy, I.R., Kim, S. and Sa, T. (2005) Wheat root colonization and nitrogenase activity by Azospirillum brasilense isolates from crop plants in Korea. Can J Microbiol 51, 948-956.
38. Kim, Y.-C., Glick, B.R., Bashan, Y. and Ryu, C.-M. 2012. Enhancement of plant drought tolerance by microbes. In: Plant Responses to Drought Stress: from Morphological to Molecular Features ed.Aroca, R. Chapter 15. pp. 383-413. Berlin, Heidelberg, Germany: Springer Verlag.
39. Kohler, J., Hernández, J.A., Caravaca, F. and Roldán, A. (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65, 245-252.
40. Kolenbrander, P.E., Ganeshkumar, N., Cassels, F.J. and Hughes, C.V. (1993) Coaggregation: specific adherence among human oral plaque bacteria. FASEB J 7, 406-413.
41. Kumar, K.B. and Khan, P.A. (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine coracana cv. PR 202) leaves during senescence. Ind J Exp Bot 20, 412-416.
42. Lee, M., Chauhan, P.S., Yim, W., Lee, G., Kim, Y.S., Park, K. and Sa, T. (2011) Foliar colonization and growth promotion of red pepper (Capsicum annuum L.) by Methylobacterium oryzae CBMB20. J Appl Biol Chem 54, 120-125.
43. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
44. Madhaiyan, M., Poonguzhali, S., Ryu, J.H. and Sa, T. (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane- 1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224, 268-278.
45. Madhaiyan, M., Poonguzhali, S. and Sa, T. (2007) Characterization of 1-aminocyclopropane-1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 226, 867-876.
46. Madhaiyan, M., Poonguzhali, S., Kang, B.-G., Lee, Y.-J., Chung, J.-B. and Sa, T. (2010) Effect of co-inoculation of methylotrophic Methylobacterium oryzae with Azospirillum brasilense and Burkholderia pyrrocinia on the growth and nutrient uptake of tomato, red pepper and rice. Plant Soil 328, 71-82.
47. Manachini, P.L., Parini, C. and Fortina, G. (1988) Pectic enzymes from Aureobasidium pullulans LV 10. Enzyme Microb Technol 10, 682-685.
48. Neyra, C.A., Atkinson, A. and Olubayi, O. (1995) Coaggregation of Azospirillum brasilense with other bacteria: basis for functional diversity. NATO ASI Series G Ecol Sci 37, 429-439.
49. Neyra, C.A., Arunakumari, A. and Olybayi, O. (1997) Flocculated microbial inoculants for delivery of agriculturally beneficial microorganisms, U.S Patent No. 454317.
50. Nitisinprasert, S. and Temmes, A. (1991) The characteristics of a new non-spore-forming cellulolytic mesophilic anaerobe strain CM126 isolated from municipal sewage sludge. J Appl Bacteriol 71, 154-161.
51. Okon, Y., Houchins, J.P., Albrecht, S.L. and Burris, R.H. (1977) Growth of Spirillum lipoferum at constant partial pressures of oxygen, and the properties of its nitrogenase in cell-free extracts. J Gen Microbiol 98, 87-93.
52. Pereyra, M.A., Zalazar, C.A. and Barassi, C.A. (2006) Root phospholipids in Azospirillum brasilense-inoculated wheat seedlings exposed to water stress. Plant Physiol Biochem 44, 873-879.
53. Pirttilà, A.M., Pospiech, H., Laukkanen, H., Myllyla, R. and Hohtola, A. (2005) Seasonal variations in location and population structure of endophytes in buds of Scots pine. Tree Physiol 25, 289-297.
54. Poonguzhali, S., Madhaiyan, M., Yim, W.J., Kim, K.A. and Sa, T. (2008) Colonization pattern of plant root and leaf surfaces visualized by use of green-fluorescent-marked strain of Methylobacterium suomiense and its persistence in rhizosphere. Appl Microbiol Biotechnol 78, 1033-1043.
55. Prigent-Combaret, C., Blaha, D., Pothier, J.F., Vial, L., Poirier, M.A., Wisniewski-Dye, F. and Moenne-Loccoz, Y. (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiol Ecol 65, 202-219.
56. Schmidt, C.S., Agostini, F., Simon, A.M., Whyte, J., Townend, J., Lifert, C., Killham, K. and Mullins, C. (2004) Influence of soil type and pH on the colonization of sugar beet seedlings by antagonistic Pseudomonas and Bacillus strains, and on their control of Pythium damping-off. Eur J Plant Pathol 110, 1025-1046.
57. Toeda, K. and Kurane, R. (1991) Microbial flocculant from Alcaligenes cupidus KT201. Agric Biol Chem 55, 2793-2799.
58. Trejo, A., de-Bashan, L. E., Hartmann, A., Hernandez, J.P., Rothballer, M., Schmid, M. and Bashan, Y. (2012) Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil. Env Exp Bot 75, 65-73.
59. Vaca, C.E., Wilhelm, J. and Harms-Ringdahl, M. (1988) Interaction of lipid peroxidation products with DNA-A review. Mutat Res 195, 137-149.
60. Verma, S.C., Ladha, J.K. and Tripathi, A.K. (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91, 127-141.
61. Whittenbury, R., Davies, S.L. and Wilkinson, J.F. (1970) Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61, 205-218.
62. Yim, W., Seshadri, S., Kim, K., Lee, G. and Sa, T. (2013) Ethylene emission and PR protein synthesis in ACC deaminase producing Methylobacterium spp. inoculated tomato plants (Lycopersicon esculentum Mill.) challenged with Ralstonia solanacearum under greenhouse conditions. Plant Physiol Biochem 67, 95-104.