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Ecological Occurrence of Gluconacetobacter diazotrophicus and Nitrogen-fixing Acetobacteraceae Members: Their Possible Role in Plant Growth Promotion

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Abstract

Gluconacetobacter diazotrophicus has a long-standing history of bacterial-plant interrelationship as a symbiotic endophyte capable of fixing atmospheric nitrogen. In low nitrogen fertilized sugarcane fields it plays a significant role and its occurrence was realised in most of the sugarcane growing countries. In this mini review, the association of G. diazotrophicus with sugarcane, other crop plants and with various hosts is discussed. The factors affecting survival in the rhizosphere and the putative soil mode of transmission are emphasized. In addition, other N2-fixing Acetobacteraceae members, including Gluconacetobacter azotocaptans, Gluconacetobacter johannae and Swaminathania salitolerans, occurring in coffee, corn and rice plants are also covered. Lastly, the plant-growth-promoting traits identified in this group of bacteria, including N2 fixation, phytohormone synthesis, P and Zn solubilization and biocontrol, are analysed.

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References

  1. Adriano-Anaya, M, Salvador-Figueroa, M, Ocampo, JA, García-Romera, I (2005) Plant cell-wall degrading hydrolytic enzymes of Gluconacetobacter diazotrophicus. Symbiosis 40: 151–156

    CAS  Google Scholar 

  2. Adriano-Anaya, ML, Salvador-Figueroa, M, Ocampo, JA, García-Romera, I (2006) Hydrolytic enzyme activities in maize (Zea mays) and sorghum (Sorghum bicolor) roots inoculated with Gluconacetobacter diazotrophicus and Glomus intraradices. Soil Biol Biochem 38: 879–886

    CAS  Google Scholar 

  3. Alvarez, B, Martinez-Drets, G (1995) Metabolic characterization of Acetobacter diazotrophicus. Can J Microbiol 41: 918–924

    Article  CAS  Google Scholar 

  4. Ando, S, Goto, M, Meunchang, S, Thongra-ar, P, Fujiwara, T, Hayashi, H, Yoneyama, T (2005) Detection of nifH sequences in sugarcane (Saccharum officinarum L.) and pineapple (Ananas comosus [L.] Merr.). Soil Sci Plant Nutr 51: 303–308

    CAS  Google Scholar 

  5. Ashbolt, NJ, Inkerman, PA (1990) Acetic acid bacterial biota of the pink sugarcane mealybug, Saccharococcus sacchari, and its environs. Appl Environ Microbiol 56: 707–712

    PubMed  CAS  Google Scholar 

  6. Asis, CA, Jr, Kubota, M, Chebotar, VK, Ohta, H, Arima, Y, Nishiyama, K, Tsuchiya, K, Akao, S (2000) Endophytic bacterial population in Philippine sugarcane cultivars and isolation of nitrogen-fixing strains. Microbes Environ 15: 209–216

    Google Scholar 

  7. Asis, CA, Jr, Kubota, M, Ohta, H, Arima, Y, Chebotar, VK, Tsuchiya, K, Akao, S (2000) Isolation and partial characterization of endophytic diazotrophs associated with Japanese sugarcane cultivar. Soil Sci Plant Nutr 46: 759–765

    Google Scholar 

  8. Baldani, JI, Caruso, L, Baldani, VLD, Goi, SR, Döbereiner, J (1997) Recent advances in BNF with non-legume plants. Soil Biol Biochem 29: 911–922

    CAS  Google Scholar 

  9. Baldani, JI, Reis, VM, Baldani, VLD, Döbereiner, J (2002) A brief story of nitrogen fixation in sugarcane-reasons for success in Brazil. Funct Plant Biol 29: 417–423

    Google Scholar 

  10. Baldani, JI, Baldani, VLD (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Ciênc 77: 549–579

    PubMed  CAS  Google Scholar 

  11. Bansal, RK, Dahiya, RS, Narula, N, Jain, RK (2005) Management of Meloidogyne incognita in cotton using strains of the bacterium Gluconacetobacter diazotrophicus. Nematol Mediter 33: 101–105

    Google Scholar 

  12. Bastián, F, Cohen, A, Piccoli, P, Luna, V, Baraldi, R, Bottini, R (1998) Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically defined culture media. Plant Growth Regul 24: 7–11

    Google Scholar 

  13. Blanco, Y, Blanch, M, Piñón, D, Legaz, ME, Vicente, C (2005) Antagonism of Gluconacetobacter diazotrophicus (a sugarcane endosymbiont) against Xanthomonas albilineans (pathogen) studied in alginate-immobilized sugarcane stalk tissues. J Biosci Bioeng 99: 366–371

    PubMed  CAS  Google Scholar 

  14. Boddey, RM, Urquiaga, S, Reis, VM, Döbereiner, J (1991) Biological nitrogen fixation associated with sugarcane. Plant Soil 37: 111–117

    Google Scholar 

  15. Boddey, RM, de Oliveira, OC, Urquiaga, S, Reis, VM, de Olivares, FL, Baldani, VLD, Döbereiner J (1995) Biological nitrogen fixation associated with sugarcane and rice: Contributions and prospects for improvement. Plant Soil 174: 195–209

    CAS  Google Scholar 

  16. Boddey, RM, Urquiaga, S, Alves, BJR, Reis, VM (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252: 139–149

    CAS  Google Scholar 

  17. Caballero-Mellado, J, Fuentes-Ramírez, LE, Reis, VM, Martínez-Romero, E (1995). Genetic structure of Acetobacter diazotrophicus populations and identification of a new genetically distant group. Appl Environ Microbiol 61: 3008–3013

    PubMed  CAS  Google Scholar 

  18. Carrizo de Bellone, S, Bellone, CH (2006) Presence of endophytic diazotrophs in sugarcane juice. World J Microbiol Biotechnol 22: 1065–1068

    Google Scholar 

  19. Cavalcante, VA, Döbereiner, J (1988) A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108: 23–31

    Google Scholar 

  20. Cavalcante, JJV, Vargas, C, Nogueira, EM, Vinagre, F, Schwarcz, K, Baldani, JI, Ferreira PCG, Hemerly, AS (2007) Members of the ethylene signalling pathway are regulated in sugarcane during the association with nitrogen-fixing endophytic bacteria. J Exp Bot 58: 673–686

    PubMed  CAS  Google Scholar 

  21. Cocking, EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252: 169–175

    CAS  Google Scholar 

  22. Cocking, EC, Stone, PJ, Davey, MR (2006) Intracellular colonization of roots of Arabidopsis and crop plants by Gluconacetobacter diazotrophicus. In Vitro Cell Dev Biol-Plant 42: 74–82

    Google Scholar 

  23. Debarry, M, Marten, I, Ngezahayo, A, Kolb, HA (2005) Differential defense responses in sweet potato suspension culture. Plant Sci 168: 1171–1179

    CAS  Google Scholar 

  24. Dobbelaere, S, Vanderleyden, J, Okon, Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22: 107–149

    CAS  Google Scholar 

  25. Döbereiner, J, Reis, VM, Lazarini, AC (1988) New N2 fixing bacteria in association with cereals and sugarcane. In: Bothe, H, de Bruijn, FJ, Newton, WE (Eds.) Nitrogen Fixation: Hundred Years After. Gustav Fisher, Stuttgart, pp 717–722

    Google Scholar 

  26. Döbereiner, J, Pimentel, P, Olivares, FL, Urquiaga, S (1990) Batéria diazotrofica podem J ser endófitas e ou fitopatogénicas. An Acad Bras Ciênc 62: 319

    Google Scholar 

  27. Döbereiner, J, Reis, VM, Paula, MA, Olivares, FL (1993) Endophytic diazotrophs in sugarcane, cereals and tuber plants. In: Palacios, R, Mora, J, Newton, WE (Eds.) New Horizons in Nitrogen Fixation. Kluwer, Dordrecht, pp 671–676

    Google Scholar 

  28. Dong, Z, Canny, MJ, McCully, ME, Roboredo, MR, Cabadilla, CF, Ortega, E, Rodes, R (1994) A nitrogen fixing endophyte of sugarcane stems. (A new role for the apoplast). Plant Physiol 105: 1139–1147

    PubMed  CAS  Google Scholar 

  29. Dong, Z, Heydrich, M, Bernard, K, McCully, ME (1995) Further evidence that the N2 fixing endophytic bacterium from the intercellular spaces of sugarcane stems is Acetobacter diazotrophicus. Appl Environ Microbiol 61: 1843–1846

    PubMed  CAS  Google Scholar 

  30. Dong, Z, McCully, ME, Canny, MJ (1997) Does Acetobacter diazotrophicus live and move in the xylem of sugarcane stems? Anatomical and physiological data. Ann Bot 80: 147–158

    Google Scholar 

  31. Dong, Z, Zelmer, CD, Canny, MJ, McCully, ME, Luit, B, Pan, B, Faustino, RS, Pierce, GN, Vessey, JK (2002) Evidence for protection of nitrogenase from O2 by colony structure in the aerobic diazotroph Gluconacetobacter diazotrophicus. Microbiology-(UK) 148: 2293–2298

    CAS  Google Scholar 

  32. Dutta, D, Gachhui, R (2006) Novel nitrogen-fixing Acetobacter nitrogenifigens sp. nov., isolated from Kombucha tea. Int J Sys Evol Microbiol 56: 1899–1903

    CAS  Google Scholar 

  33. Dutta, D, Gachhui, R (2007) Nitrogen-fixing and cellulose-producing Gluconacetobacter kombuchae sp. nov. isolated from Kombucha tea. Int J Syst Evol Microbiol 57: 353–357

    PubMed  CAS  Google Scholar 

  34. Emtiazi, G, Etemadifar, Z, Tavassoli, M (2003) A novel nitrogen-fixing cellulytic bacterium associated with root of corn is a candidate for production of single cell protein. Biomass Bioenergy 25: 423–426

    CAS  Google Scholar 

  35. Fisher, K, Newton, WE (2005) Nitrogenase proteins from Gluconacetobacter diazotrophicus, a sugarcane-colonizing bacterium. BBA-Proteins Proteomics 1750: 154–165

    CAS  Google Scholar 

  36. Flores-Encarnación, M, Contreras-Zentella, M, Soto-Urzua, L, Aguilar, GR, Baca, BE, Escamilla, JE (1999) The respiratory system and diazotrophic activity of Acetobacter diazotrophicus PAL5. Appl Environ Microbiol 181: 6987–6995

    Google Scholar 

  37. Franke, IH, Fegan, M, Hayward, C, Leonard, G, Stackebrandt, E, Sly, LI (1999) Description of Gluconacetobacter sacchari sp. nov., a new species of acetic acid bacterium isolated from the leaf sheath of sugarcane and from the pink sugarcane mealybug. Int J Syst Bacteriol 49: 1681–1693

    Article  PubMed  CAS  Google Scholar 

  38. Franke-Whittle, IH, O’Shea, MG, Leonard, GJ, Webb, R, Sly, LI (2005) Investigation into the ability of Gluconacetobacter sacchari to live as an endophyte in sugarcane. Plant Soil 271: 285–295

    CAS  Google Scholar 

  39. Franke-Whittle, IH, O’Shea, MG, Leonard, GJ, Sly, LI (2005) Design, development, and use of molecular primers and probes for the detection of Gluconacetobacter species in the pink sugarcane mealybug. Microb Ecol 50: 128–139

    PubMed  CAS  Google Scholar 

  40. Fuentes, R, Tapia, H, Jiménez, S, Mascarúa, E, Santoyo, P, Caso, V, Romero, H, Cajica, E, León, B, Rosales, P, Füguemann, M, Castillo, R (2003) Bacterias acéticas: Diversidad e interacción con las plantas. Elementos: ciencia y cultura 10: 47–51

    Google Scholar 

  41. Fuentes-Ramírez, LE, Jiménez-Salgado, T, Abarca-Ocampo, IR, Caballero-Mellado, J (1993) Acetobacter diazotrophicus, an indole acetic acid producing bacterium isolated from sugarcane cultivars of Mexico. Plant Soil 154: 145–150

    Google Scholar 

  42. Fuentes-Ramírez, LE, Caballero-Mellado, J, Sepúlveda, J, Martínez-Romero, E (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol Ecol 29: 117–129

    Google Scholar 

  43. Fuentes-Ramírez, LE, Bustillos-Cristales, R, Tapia-Hernández, A, Jiménez-Salgado, T, Wang, ET, Martínez-Romero, E, Caballero-Mellado, J (2001) Novel nitrogen-fixing acetic acid bacteria Gluconacetobacter johannae sp. nov. and Gluconacetobacter azotocaptans sp. nov., associated with coffee plants. Int J Syst Evol Microbiol 51: 1305–1314

    PubMed  Google Scholar 

  44. Gillis, M, Kersters, K, Hoste, B, Janssens, D, Kroppenstedt, RM, Stephan, MP, Teixeira, KRS, Döbereiner, J, De Ley, J (1989) Acetobacter diazotrophicus sp. nov., a nitrogen fixing acetic acid bacterium associated with sugarcane. Int J Syst Bacteriol 39: 361–364

    Google Scholar 

  45. González, B, Martínez, S, Chávez, JL, Lee, S, Castro, NA, Domínguez, MA, Gómez, S, Contreras, ML, Kennedy, C, Escamilla, JE (2006) Respiratory system of Gluconacetobacter diazotrophicus PAL5 evidence for a cyanide-sensitive cytochrome bb and cyanide-resistant cytochrome ba quinol oxidases. Biochim Biophys Acta Bioenerg 1757: 1614–1622

    Google Scholar 

  46. Govindarajan, M, Balandreau, J, Muthukumarasamy, R, Revathi, G, Lakshminarasimhan, C (2006). Improved yield of micropropagated sugarcane following inoculation by endophytic Burkholderia vietnamiensis. Plant Soil 280: 239–252

    CAS  Google Scholar 

  47. Greenberg, DE, Porcella, SF, Stock, F, Wong, A, Conville, PS, Murray, PR, Holland, SM, Zelazny, AM (2006) Granulibacter bethesdensis gen. nov., sp. nov., a distinctive pathogenic acetic acid bacterium in the family Acetobacteraceae. Int J Syst Evol Microbiol 56: 2609–2616

    PubMed  CAS  Google Scholar 

  48. Hoefsloot, G, Termorshuizen, AJ, Watt, DA, Cramer, MD (2005) Biological nitrogen fixation is not a major contributor to the nitrogen demand of a commercially grown South African sugarcane cultivar. Plant Soil 277: 85–96

    CAS  Google Scholar 

  49. James, EK, Reis, VM, Olivares, FL, Baldani, JI, Döbereiner, J (1994) Infection of sugarcane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J Exp Bot 45: 757–766

    CAS  Google Scholar 

  50. James, EK, Olivares, FL (1998) Infection and colonization of sugarcane and other graminaceous plants by endophytic diazotrophs. Crit Rev Plant Sci 17: 77–119

    Google Scholar 

  51. James, EK, Olivares, FL, de Oliveira, ALM, dos Reis, Jr, FB, da Silva, LG, Reis, VM (2001) Further observations on the interaction between sugarcane and Gluconacetobacter diazotrophicus under laboratory and greenhouse conditions. J Exp Bot 52: 747–760

    PubMed  CAS  Google Scholar 

  52. Jiménez-Salgado, T, Fuentes-Ramírez, LE, Tapia-Hernández, A, Mascarua, MA, Martínez-Romero, E, Caballero-Mellado, J (1997) Coffea arabica L., a new host plant for Acetobacter diazotrophicus, and isolation of other nitrogen fixing acetobacteria. Appl Environ Microbiol 63: 3676–3683

    PubMed  Google Scholar 

  53. Kersters, K, Lisdiyanti, P, Komagata, K, Swings, J (2006) The Family Acetobacteraceae: The genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia. In: Dworkin, M, Falkow, S, Rosenberg, E, Schleifer, KH, Stackebrandt, E (Eds.) The Prokaryotes (3rd Edn.): A Handbook on the Biology of Bacteria: Proteobacteria: Alpha and Beta sub classes Vol 5, Springer, New York, pp 163–200

    Google Scholar 

  54. Kuklinsky-Sobral, J, Araújo, WL, Mendes, R, Geraldi, IO, Pizzirani-Kleiner, AA, Azevedo, JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 12: 1244–1251

    Google Scholar 

  55. Lee, S, Sevilla, M, Reth, A, Meletzus, D, Gunapala, N, Kennedy, C (2000) Characterization of nitrogen fixation genes and plant-growth promoting properties in Acetobacter diazotrophicus, an endophyte of sugarcane. In: Stacey, G, Keen, NT (Eds.) Plant-Microbe Interactions, APS Press, St. Paul, pp 297–314

    Google Scholar 

  56. Lee, S, Reth, A, Meletzus, D, Sevilla, M, Kennedy, C (2000) Characterization of a major cluster of nif, fix, and associated genes in a sugarcane endophyte, Acetobacter diazotrophicus. J Bacteriol 182: 7088–7091

    PubMed  CAS  Google Scholar 

  57. Lee, S, Flores-Encarnación, M, Contreras-Zentella, M, Garcia-Flores, L, Escamilla, JE, Kennedy, C (2004) Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome c biogenesis genes. J Bacteriol 186: 5384–5391

    PubMed  CAS  Google Scholar 

  58. Li, RP, Macrae, IC (1991) Specific association of diazotrophic acetobacters with sugarcane. Soil Biol Biochem 23: 999–1002

    CAS  Google Scholar 

  59. Loganathan, P, Sunitha, R, Parida, AK, Nair, S (1999) Isolation and characterization of two genetically distant groups of Acetobacter diazotrophicus from a new host plant Eleusine coracana L. J Appl Microbiol 87: 167–172

    Google Scholar 

  60. Loganathan, P, Nair, S (2003) Crop-specific endophytic colonization by a novel, salt-tolerant, N2 fixing and phosphate-solubilizing Gluconacetobacter sp. from wild rice. Biotechnol Lett 25: 497–501

    PubMed  CAS  Google Scholar 

  61. Loganathan, P, Nair, S (2004) Swaminathania salitolerans gen. nov., sp. nov., a salt tolerant, nitrogen fixing and phosphate-solubilizing bacterium from wild rice (Porteresia coarctata Tateoka). Int J Syst Evol Microbiol 54: 1185–1190

    PubMed  CAS  Google Scholar 

  62. Luna, MF, Mignone, CF, Boiardi, JL (2000) The carbon source influences the energetic efficiency of the respiratory chain of N2-fixing Acetobacter diazotrophicus. Appl Microbiol Biotechnol 54: 564–569

    PubMed  CAS  Google Scholar 

  63. Luna, MF, Bernardelli, CE, Mignone, CF, Boiardi, JL (2002) Energy generation by extracellular aldose oxidation in N2 fixing Gluconacetobacter diazotrophicus. Appl Environ Microbiol 68: 2054–2056

    PubMed  CAS  Google Scholar 

  64. Luna, MF, Bernardelli, CE, Galar, ML, Boiardi, JL (2006) Glucose metabolism in batch and continuous cultures of Gluconacetobacter diazotrophicus PAL 3. Curr Microbiol 52: 163–168

    PubMed  CAS  Google Scholar 

  65. Madhaiyan, M, Saravanan, VS, Bhakiya Silba Sandal Jovi, D, Lee, H, Thenmozhi, R, Hari, K, Sa, TM (2004) Occurrence of Gluconacetobacter diazotrophicus in tropical and subtropical plants of Western Ghats, India. Microbiol Res 159: 233–243

    PubMed  CAS  Google Scholar 

  66. Madhaiyan, M, Poonguzhali, S, Hari, K, Saravanan, VS, Sa, TM (2006) Influence of pesticides on the growth rate and plant-growth promoting traits of Gluconacetobacter diazotrophicus. Pest Biochem Physiol 84: 143–154

    CAS  Google Scholar 

  67. Maheshkumar, KS, Krishnaraj, PU, Alagawadi, AR (1999) Mineral phosphates solubilizing activity of Acetobacter diazotrophicus: a bacterium associated with sugarcane. Curr Sci 76: 874–875

    Google Scholar 

  68. Marchal, K, Vanderleyden, J (2000) The “oxygen paradox” of dinitrogen-fixing bacteria. Biol Fertil Soils 30: 363–373

    CAS  Google Scholar 

  69. Matiru, V, Thomson, J (1998) Can Acetobacter diazotrophicus be used as a growth promoter for coffee, tea and banana plants? In: Dakora, FD (Ed.) Proceedings of the 8th Congress of the African Association for Biological Nitrogen Fixation. University of Cape Town, South Africa, pp 129–130

  70. Medeiros, AFA, Polidoro, JC, Reis, VM (2006) Nitrogen source effect on Gluconacetobacter diazotrophicus colonization of sugarcane (Saccharum spp.). Plant Soil 279: 141–152

    CAS  Google Scholar 

  71. Mehnaz, S, Lazarovits, G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51: 326–335

    PubMed  Google Scholar 

  72. Mehnaz, S, Weselowski, B, Lazarovits, G (2006) Isolation and identification of Gluconacetobacter azotocaptans from corn rhizosphere. Syst Appl Microbiol 29: 496–501

    PubMed  CAS  Google Scholar 

  73. Meletzus, D, Teixeira, K, Perlova, O, Nawroth, R, Zellermann, E, Morgan, T, Baldani, IV, Kennedy, C (1998) Characterization of genes involved in regulation of nitrogen fixation and ammonium sensing in Acetobacter diazotrophicus, an endophyte of sugarcane. In: Elmerich, C, Kondorosi, A, Newton, WE (Eds.) Biological Nitrogen Fixation for the 21st Century. Kluwer, Dordrecht, pp 125–126

    Google Scholar 

  74. Moutia, JFY, Umrit, G, Saumtally, AS, Ng Kee Kwong, KF (2003) The role of diazotrophic bacteria in the nitrogen nutrition of sugarcane in Mauritius: preliminary results. AMAS Food and Agricultural Research Council, Réduit, pp 29–39

    Google Scholar 

  75. Muñoz-Rojas, J, Caballero-Mellado, J (2003) Population dynamics of Gluconacetobacter diazotrophicus in sugarcane cultivars and its effect on plant growth. Microb Ecol 46: 454–564

    PubMed  Google Scholar 

  76. Muñoz-Rojas, J, Fuentes-Ramírez, LE, Caballero-Mellado, J (2005) Antagonism among Gluconacetobacter diazotrophicus strains in culture media and in endophytic association. FEMS Microbiol Ecol 54: 57–66

    PubMed  Google Scholar 

  77. Muthukumarasamy, R, Revathi, G, Lakshminarasimhan, C (1999) Influence of N fertilization on the isolation of Acetobacter diazotrophicus and Herbaspirillum spp. from Indian sugarcane varieties. Biol Fertil Soils 29: 157–164

    CAS  Google Scholar 

  78. Muthukumarasamy, R, Revathi, G (1999) Diazotrophic associations in sugarcane cultivation in South India. Trop Agric (Trinidad) 76: 171–178

    Google Scholar 

  79. Muthukumarasamy, R, Revathi, G, Vadivelu, M (2000) Antagonistic potential of N2 fixing Acetobacter diazotrophicus against Colletotrichum falcatum Went, a causal organism of red-rot of sugarcane. Curr Sci 78: 1063–1065

    Google Scholar 

  80. Muthukumarasamy, R, Revathi, G, Loganathan, P (2002) Effect of inorganic N on the population, in vitro colonization and morphology of Acetobacter diazotrophicus (syn. Gluconacetobacter diazotrophicus). Plant Soil 243: 91–102

    CAS  Google Scholar 

  81. Muthukumarasamy, R, Cleenwerck, I, Revathi, G, Vadivelu, M, Janssens, D, Hoste, B, Gum, KU, Park, KD, Son, CY, Sa, TM, Caballero-Mellado, J (2005) Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28: 277–286

    PubMed  CAS  Google Scholar 

  82. Muthukumarasamy, R, Govindarajan, M, Vadivelu, M, Revathi, G (2006) N-fertilizer saving by the inoculation of Gluconacetobacter diazotrophicus and Herbaspirillum sp. in micropropagated sugarcane plants. Microbiol Res 161: 238–245

    PubMed  CAS  Google Scholar 

  83. Muthukumarasamy, R, Kang, UG, Park, KD, Jeon, WT, Park, CY, Cho, YS, Kwon, SW, Song, J, Roh, DH, Revathi, G (2007) Enumeration, isolation and identification of diazotrophs from Korean wetland rice varieties grown with long-term application of N and compost and their short-term inoculation effect on rice plants. J Appl Microbiol 102: 981–991

    PubMed  CAS  Google Scholar 

  84. Nogueira, EM, Vinagre, F, Masuda, HP, Vargas, C, Pádua,VLMD, Silva, FRD, Santos, RVD, Baldani, JI, Ferreira, PCG, Hemerly, AS (2001) Expression of sugarcane genes induced by inoculation with Gluconacetobacter diazotrophicus and Herbaspirillum rubrisubalbicans. Genet Mol Biol 24: 199–206

    CAS  Google Scholar 

  85. Oliveira, ALM, Urquiaga, S, Döbereiner, J, Baldani, JI (2002) The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants. Plant Soil 242: 205–215

    CAS  Google Scholar 

  86. Oliveira, ALM, Canuto, EL, Silva, EE, Reis, VM, Baldani, JI (2004) Survival of endophytic diazotrophic bacteria in soil under different moisture levels. Braz J Microbiol 35: 295–299

    Google Scholar 

  87. Oliveira, ALM, Canuto, EDL, Urquiaga, S, Reis, VM, Baldani, JI (2006) Yield of micropropagated sugarcane varieties in different soil types following inoculation with diazotrophic bacteria. Plant Soil 284: 23–32

    CAS  Google Scholar 

  88. Paula, MA, Reis, VM, Döbereiner, J (1991) Interactions of Glomus clarum with Acetobacter diazotrophicus in infection of sweet potato (Ipomea batatus), sugarcane (Saccharum sp.) and sweet sorghum (Sorghum bicolor). Biol Fertil Soils 11: 111–115

    Google Scholar 

  89. Perlova, O, Nawroth, R, Zellermann, EM, Meletzus, D (2002) Isolation and characterization of the glnD gene of Gluconacetobacter diazotrophicus, encoding a putative uridylyltransferase/uridylyl-removing enzyme. Gene 297: 159–168

    PubMed  CAS  Google Scholar 

  90. Perlova, O, Ureta, A, Nordlund, S, Meletzus, D (2003) Identification of three genes encoding PII-like proteins in Gluconacetobacter diazotrophicus: studies of their role(s) in the control of nitrogen fixation. J Bacteriol 185: 5854–5861

    PubMed  CAS  Google Scholar 

  91. Piñón, D, Casas, M, Blanch, M, Fontaniella, B, Blanco, Y, Vicente, C, Solas, MT, Legaz, ME (2002) Gluconacetobacter diazotrophicus, a sugarcane endosymbiont, produces a bacteriocin against Xanthomonas albilineans, a sugarcane pathogen. Res Microbiol 153: 345–351

    PubMed  Google Scholar 

  92. Reis Junior, FB, Reis, VM, Urquiaga, S, Döbereiner, J (2000) Influence of nitrogen fertilization on the population of diazotrophic bacteria Herbaspirillum spp. and Acetobacter diazotrophicus in sugarcane (Saccharum spp.). Plant Soil 219: 153–159

    Google Scholar 

  93. Saravanan, VS (2004) An investigation on solubilization of zinc and certain other insoluble compounds by Gluconacetobacter diazotrophicus. Ph.D. thesis, Tamil Nadu Agricultural University, Coimbatore, p 130

  94. Saravanan, VS, Madhaiyan, M, Thangaraju, M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66: 1794–1798

    PubMed  CAS  Google Scholar 

  95. Saravanan, VS, Kalaiarasan, P, Madhaiyan, M, Thangaraju, M (2007) Solubilization of insoluble zinc compounds by Gluconacetobacter diazotrophicus and the detrimental action of zinc ion (Zn2+) and zinc chelates on root knot nematode Meloidogyne incognita. Lett Appl Microbiol 44: 235–241

    PubMed  CAS  Google Scholar 

  96. Sevilla, M, Meletzus, D, Teixeira, K, Lee, S, Nutakki, A, Baldani, I, Kennedy, C (1997) Analysis of nif and regulatory genes in Acetobacter diazotrophicus. Soil Biol Biochem 29: 871–874

    CAS  Google Scholar 

  97. Sevilla, M, Burris, RH, Gunapala, N, Kennedy, C (2001) Comparison of benefit to sugarcane plant growth and 15N2 incorporation following inoculation of sterile plants with Acetobacter diazotrophicus wild-type and nif mutant strains. Mol Plant-Microbe Interact 14: 358–366

    PubMed  CAS  Google Scholar 

  98. Stephan, MP, Oliveira, M, Teixeira, KRS, Martínez-Drets, G, Döbereiner, J (1991) Physiology and dinitrogen fixation of Acetobacter diazotrophicus. FEMS Microbiol Lett 77: 67–72

    CAS  Google Scholar 

  99. Suman, A, Shasany, AK, Singh, M, Shahi, HN, Gaur, A, Khanuja, SPS (2001) Molecular assessment of diversity among endophytic diazotrophs isolated from subtropical Indian sugarcane. World J Microbiol Biotechnol 17: 39–45

    CAS  Google Scholar 

  100. Suman, A, Gaur, A, Shrivastava, AK, Yadav, RL (2005) Improving sugarcane growth and nutrient uptake by inoculating Gluconacetobacter diazotrophicus. Plant Growth Regul 47: 155–162

    CAS  Google Scholar 

  101. Snyder, RW, Ruhe, J, Kobrin, S, Wasserstein, A, Doline, C, Nachamkin, I, Lipschutz, JH (2004) Asaia bogorensis peritonitis identified by 16S ribosomal RNA sequence analysis in a patient receiving peritoneal dialysis. Am J Kidney Dis 44: e15–e17

    PubMed  Google Scholar 

  102. Tapia-Hernández, A, Bustillos-Cristales, MR, Jiménez-Salgado, T, Caballero-Mellado, J, Fuentes-Ramírez, LE (2000) Natural endophytic occurrence of Acetobacter diazotrophicus in pineapple plants. Microb Ecol 39: 49–55

    PubMed  Google Scholar 

  103. Teixeira, KRS, Wulling, M, Morgan, T, Galler, R, Zellermann, EM, Baldani, JI, Kennedy, C, Meletzus, D (1999) Molecular analysis of the chromosomal region encoding the nifA and nifB genes of Acetobacter diazotrophicus. FEMS Microbiol Lett 176: 301–309

    CAS  Google Scholar 

  104. Tejera, N, Lluch, C, Martínez-Toledo, MV, González-López, J (2005) Isolation and characterization of Azotobacter and Azospirillum strains from the sugarcane rhizosphere. Plant Soil 270: 223–232

    CAS  Google Scholar 

  105. Tuuminen, T, Heinäsmäki, T, Kerttula, T (2006) First report of bacteremia by Asaia bogorensis, in a patient with a history of intravenous-drug abuse. J Clin Microbiol 44: 3048–3050

    PubMed  Google Scholar 

  106. Ureta, A, Nordlund, S (2001) Glutamine synthetase from Acetobacter diazotrophicus: properties and regulation. FEMS Microbiol Lett 202: 177–180

    PubMed  CAS  Google Scholar 

  107. Ureta, A, Nordlund, S (2002) Evidence for conformational protection of nitrogenase against oxygen in Gluconacetobacter diazotrophicus by a putative FeSII Protein. J Bacteriol 184: 5805–5809

    PubMed  CAS  Google Scholar 

  108. Vinagre, F, Vargas, C, Schwarcz, K, Cavalcante, J, Nogueira, EM, Baldani, JI, Ferreira, PCG, Hemerly, AS (2006) SHR5: a novel plant receptor kinase involved in plant-N2-fixing endophytic bacteria association. J Exp Bot 57: 559–569

    PubMed  CAS  Google Scholar 

  109. Vargas, C, Pádua, VLMD, Nogueira, EDM, Vinagre, F, Masuda, HP, Silva, FRD, Baldani, JI, Ferreira, PCG, Hemerly, AS (2003) Signaling pathways mediating the association between sugarcane and endophytic diazotrophic bacteria: a genomic approach. Symbiosis 35: 159–180

    CAS  Google Scholar 

  110. Yamada, Y, Hoshino, KI, Ishikawa, T (1998) Gluconacetobacter nom.corrig. Gluconacetobacter (sic). In: validation of publication of new names and new combinations previously effectively published out side the IJSB. List no. 64. Int J Syst Bacteriol 48: 327–328

  111. Youssef, HH, Fayez, M, Monib, M, Hegazi, N (2004) Gluconacetobacter diazotrophicus: a natural endophytic diazotroph of Nile delta sugarcane capable of establishing an endophytic association with wheat. Biol Fertil Soils 39: 391–397

    CAS  Google Scholar 

  112. Walsh, KB, Brown, SM, Harrison, DK (2006) Can a N2 fixing Gluconacetobacter diazotrophicus association with sugarcane be achieved. Aust J Agric Res: 57: 235–241

    CAS  Google Scholar 

  113. Wiggins, LF (1952) Chromatography of cane non-sugars. Int Sugar J 54: 324–326

    CAS  Google Scholar 

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Acknowledgements

This paper is dedicated in memory of Johanna Döbereiner, who was the discoverer of G. diazotrophicus and eminent soil microbiologist of Brazil. We thank S. Poonguzhali and R. Anandham, Chungbuk National University for the critical reading of the manuscript. CSIR-UGC, India is gratefully acknowledged for their financial support and V.S.S. was supported as a postdoctoral fellow under the Brain Korea 21 programme, Korea Research Foundation, Republic of Korea. This work was supported by the research grant of Chungbuk National University 2006.

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Saravanan, V., Madhaiyan, M., Osborne, J. et al. Ecological Occurrence of Gluconacetobacter diazotrophicus and Nitrogen-fixing Acetobacteraceae Members: Their Possible Role in Plant Growth Promotion. Microb Ecol 55, 130–140 (2008). https://doi.org/10.1007/s00248-007-9258-6

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