The Family Rhizobiaceae

  • Lucia Maria Carareto Alves
  • Jackson Antônio Marcondes de Souza
  • Alessandro de Mello Varani
  • Eliana Gertrudes de Macedo Lemos
Reference work entry


Rhizobiaceae is a family of Rhizobiales order into Alphaproteobacteria class that presents genera associated with soil and planta hosts. Rhizobium is the type genus and encompasses the largest number of species into the family. Taxonomy is mostly supported by phylogenetic analyses based on 16S rRNA sequences and nomenclature in Rhizobiaceae is one issue that has caused much discussion. Bacteria are phenotypically heterogeneous, predominately aerobic, and Gram-negative rod-shaped. Many species present large plasmids which harbor a large proportion of genome generally including genes involved in interaction with specific hosts. Some members of the Rhizobiaceae family are characterized by their ability to establish symbiotic associations with host plants and develop the process of biological nitrogen fixation. In contrast, others are able to establish pathogenicity against plants. Both skills can be exploited for applied purposes. The selection of efficient strains from Rhizobium and Ensifer designed to plant inoculants is one of important research viewing the production of microbial inoculants to help plant development. Considering Agrobacterium tumesfaciens, the management of its natural ability to transform plants is directed to obtaining disarmed strains and clone vectors widely applied to recombinant DNA technology and plant biotechnology. Finally, some genera in Rhizobiaceae family have intriguing metabolisms which allow degradation of potentially toxic molecules and thus could be applied as biomarkers or in bioremediation.


Hairy Root Lateral Gene Transfer Crown Gall Biological Nitrogen Fixation Leguminous Plant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abd-Alla MH, Morsy FM, El-Enany AE, Ohyama T (2012) Isolation and characterization of a heavy-metal-resistant isolate of Rhizobium leguminosarum bv. viciae potentially applicable for biosorption of Cd2+ and Co2+. Int Biodeter Biodegr 67:48–55CrossRefGoogle Scholar
  2. Albuquerque P, Mendes MV, Santos CL, Moradas-Ferreira P, Tavares F (2009) DNA signature-based approaches for bacterial detection and identification. Sci Total Environ 407:3641–3651PubMedCrossRefGoogle Scholar
  3. Althabegoiti MJ, Ormeño-Orrillo E, Lozano L, Torres Tejerizo G, Rogel MA, Mora J, Martínez-Romero E (2014) Characterization of Rhizobium grahamii extrachromosomal replicons and their transfer among rhizobia. BMC Microbiol 14:6PubMedCentralPubMedCrossRefGoogle Scholar
  4. An DS, Im WT, Yang HC, Lee ST (2006) Shinella granuli gen. nov., sp. nov., and proposal of the reclassification of Zoogloea ramigera ATCC 19623 as Shinella zoogloeoides sp. nov. Int J Syst Evol Microbiol 56:443–448PubMedCrossRefGoogle Scholar
  5. Aranda-Selverio G, Barretto Penna AL, Campos-Sás LF, Santos O Jr, Vasconcelos AFD, Silva MLC, Lemos EGM, Campanharo JC, Silveira JLM (2010) Propriedades reológicas e efeito da adição de sal na viscosidade de exopolissacarídeos produzidos por bactérias do gênero Rhizobium. Quim Nova 33:895–899CrossRefGoogle Scholar
  6. Atlas RM (1997) Principles of microbiology. WCB/McGraw-Hill, SalemGoogle Scholar
  7. Auling G, Busse HJ, Egli T, El-Banna T, Stackebrand TE (1993) Description of the gram-negative, obligately aerobic, nitrilotriacetate (NTA)-utilizing bacteria as Chelatobacter heintzii, gen. nov., sp. nov., and Chelatococcus saccharovorans, gen. nov., sp. nov. Syst Appl Microbiol 16:104–112, VALIDATION LIST no. 46. Int. J. Syst. Bacteriol., 1993, 43, 624–625CrossRefGoogle Scholar
  8. Balkwill DL (2005) Genus VI Ensifer. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology,volume two the proteobacteria, part C the alpha-, beta-, delta-, and Epsilonproteobacteria. Springer, New York, pp 354–358CrossRefGoogle Scholar
  9. Batut J, Terzaghi B, Gherardi M, Huguet M, Terzaghi E, Garnerone AM, Boistard P, Huguet T (1985) Localization of a symbiotic fix region on Rhizobium meliloti pSym megaplasmid more than 200 kilobases from the nod-nif region. Mol Gen Genet 199:232–239CrossRefGoogle Scholar
  10. Bécquer CJ (2004) Descripción y clasificación de rizobios: enfoque histórico, métodos y tendencias actuales. Rev Biol 18:9Google Scholar
  11. Becker A, Pühler A (1998) Production of exopolysaccharides. In: Spaink HP, Kondorosi A, Hooykaas JJ (eds) The Rhizobiaceae. Kluwer, Dordrecht, pp 97–118CrossRefGoogle Scholar
  12. Beijerinck MW (1888) Die Bacterien der Papilionaceen-knollchen. Botanische Zeitung 46:797–804Google Scholar
  13. Beijerinck MW (1898) Über die Arten der Essigbakterien. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt II 4:209–216Google Scholar
  14. Brisbane PG, Kerr A (1983) Selective media for 3 biovars of Agrobacterium. J Appl Bacteriol 54:425–432CrossRefGoogle Scholar
  15. Burris RH (1991) Nitrogenases. J Biol Chem 266:9339–9342PubMedGoogle Scholar
  16. Cardoso JD, Hungria M, Andrade DS (2012) Polyphasic approach for the characterization of rhizobial symbionts effective in fixing N(2) with common bean (Phaseolus vulgaris L.). Appl Microbiol Biotechnol 39:1851–1864Google Scholar
  17. Cascales E, Christie PJ (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1:137–149PubMedCrossRefGoogle Scholar
  18. Casida LE (1982) Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in soil. Int J Syst Bacteriol 32:339–345CrossRefGoogle Scholar
  19. Castellane TCL, Lemos EGDM (2007) Exopolysaccharides composition produced by rhizobia under different carbon sources. Pesqui Agropecu Bras 42:1503–1506CrossRefGoogle Scholar
  20. Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38:392–397CrossRefGoogle Scholar
  21. Conn HJ (1938) Taxonomic relationships of certain non-spore formingrods in soil. J Bacteriol 36:320–321Google Scholar
  22. Crawford NM, Kahn ML, Leustek T, Long SR (2000) Nitrogen and sulfur. In: Buchanan BB, Gruissem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, p 786Google Scholar
  23. Cypionka H, Meyer O, Schlegel HG (1980) Physiological characteristics of various species of strains of carboxydobacteria. Arch Microbiol 127:301–307CrossRefGoogle Scholar
  24. Dakora FD (2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytol 158:39–49CrossRefGoogle Scholar
  25. De Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998) Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290PubMedCrossRefGoogle Scholar
  26. De Ley J, Rassel A (1965) DNA base composition, flagellation and taxonomy of the genus Rhizobium. J Gen Microbiol 41:85–92PubMedCrossRefGoogle Scholar
  27. De Vrieze J, De Lathouwer L, Verstraete W, Boon N (2013) High-rate iron-rich activated sludge as stabilizing agent for the anaerobic digestion of kitchen waste. Water Res 47:3732–3741PubMedCrossRefGoogle Scholar
  28. Dhekney SA, Li ZT, Dutt M, Gray DJ (2008) Agrobacterium-mediated transformation of embryogenic cultures and plant regeneration in Vitis rotundifolia Michx. (muscadine grape). Plant Cell Rep 27:865–872PubMedCrossRefGoogle Scholar
  29. Donot F, Fontana A, Baccou JC, Schorr-Galindo S (2012) Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydr Polym 87:951–962CrossRefGoogle Scholar
  30. Douka CE, Xenoulis AC (1988) Beneficial effects of biological nitrogen fixation on the reduction of: I. Metal toxicity of the biomass produced. II. Radioisotope uptake following the Chernobyl Fallout. In: Bothe H, De Bruijn J, Newton WE (eds) Nitrogen fixation: hundred years after. Gustav Fisher, Stuttgart, p 812Google Scholar
  31. Dudman WF (1984) The polysaccharides and oligosaccharides of Rhizobium and the role in the infection process. In: Veeger C, Newton WE (eds) Advances in nitrogen fixation research. Nijhoff/Dr. W. Junk Publishers, The Hague, pp 397–404CrossRefGoogle Scholar
  32. Euzéby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the internet. Int J Syst Bacteriol 47:590–592PubMedCrossRefGoogle Scholar
  33. Farrand SK, van Berkum PB, Oger P (2003) Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol 53:1681–1687PubMedCrossRefGoogle Scholar
  34. Ferreira L, Sánchez-Juanes F, García-Fraile P, Rivas R, Mateos PF, Martínez-Molina E, González-Buitrago JM, Velázquez E (2011) MALDI-TOF mass spectrometry is a fast and reliable platform for identification and ecological studies of species from family Rhizobiaceae. PLoS One 6:e20223PubMedCentralPubMedCrossRefGoogle Scholar
  35. Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–346Google Scholar
  36. Franke-Whittle IH, Insam H (2013) Treatment alternatives of slaughterhouse wastes, and their effect on the inactivation of different pathogens: a review. Crit Rev Microbiol 39:139–151PubMedCentralPubMedCrossRefGoogle Scholar
  37. Fred EB, Baldwin IL, McCoy E (1932) Root nodule bacteria and leguminous plants. In: University of Wisconsin studies in science, vol 5. University of Wisconsin Press, MadisonGoogle Scholar
  38. Galibert F, Finan TM, Long SR, Pühler A, Abola P, Ampe F, Vandenbol M (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672PubMedCrossRefGoogle Scholar
  39. Garrity GM, Bell JA, Lilburn T (2005) Family VII. Bradyrhizobiaceae fam. nov. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey's manual of systematic bacteriology, volume two the proteobacteria, part C the alpha-, beta-, delta-, and epsilonproteobacteria. Springer, New York, pp 438–476Google Scholar
  40. Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30:528–537PubMedCrossRefGoogle Scholar
  41. Germida JJ, Casida LE (1983) Ensifer adhaerens predatory activity against other bacteria in soil, as monitored by indirect phage analysis. Appl Environ Microbiol 45:1380–1388PubMedCentralPubMedGoogle Scholar
  42. Glaeser SP, Galatis H, Martin K, Kämpfer P (2013) Kaistia hirudinis sp. nov, isolated from the skin of Hirudo verbena. Int J Syst Evol Microbiol 63(Pt 9):3209–3213. doi:10.1099/ijs.0.049619-0, Published online ahead of print 1 March 2013PubMedCrossRefGoogle Scholar
  43. Gohlke J, Scholz CJ, Kneitz S, Weber D, Fuchs J, Hedrich R, Deeken R (2013) DNA methylation mediated control of gene expression is critical for development of crown gall tumors. PLoS Genet 9:e1003267PubMedCentralPubMedCrossRefGoogle Scholar
  44. Graham PH (1963) Antigenic affinities of the root-nodule bacteria of legumes. Antonie Van Leeuwenhoek 29(1):281–291PubMedCrossRefGoogle Scholar
  45. Graham PH (1964) The application of computer techniques to the taxonomy of the root-nodule bacteria of legumes. J Gen Microbiol 35:511–517CrossRefGoogle Scholar
  46. Graham PH, Sadowsky MJ, Keyser HH, Barnet YM, Bradley RS, Cooper JE, De Ley DJ, Jarvis BDW, Roslycky EB, Strijdom BW, Young JPW (1991) Proposed minimal standards for the description of new genera and species of root-and stem-nodulating bacteria. Int J Syst Bacteriol 41:582–587CrossRefGoogle Scholar
  47. Gutnick LD, Bach H (2000) Engineering bacterial biopolymers for the biosorption of heavy metals, new products and novel formulations. Appl Microbiol Biotechnol 54:451–460PubMedCrossRefGoogle Scholar
  48. Harrison PW, Lower RP, Kim NK, Young JP (2010) Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid. Trends Microbiol 18:141–148PubMedCrossRefGoogle Scholar
  49. Hellriegel H, Wilfarth H (1888) Untersuchungen über die Stickstoffnahrung der Gramineon und Leguminosen. Beilageheft zu der Ztschr. Ver. Rübenzucker-Industrie Deutschen Reichs 1:234Google Scholar
  50. Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil 311:1–18CrossRefGoogle Scholar
  51. Huang KH, Chen BY, Shen FT, Young CC (2012a) Optimization of exopolysaccharide production and diesel oil emulsifying properties in root nodulating bacteria. World J Microbiol Biotechnol 28:1367–1373PubMedCrossRefGoogle Scholar
  52. Huang S, Sheng P, Zhang H (2012b) Isolation and identification of cellulolytic bacteria from the gut of Holotrichia parallela larvae (Coleoptera: Scarabaeidae). Int J Mol Sci 13:2563–2577PubMedCentralPubMedCrossRefGoogle Scholar
  53. Huang Y, Zhang J, Yu Z, Zeng Y, Chen Y (2012c) Isolation and characterization of acyl homoserine lactone-producing bacteria during an urban river biofilm formation. Arch Microbiol 194:1043–1048PubMedCrossRefGoogle Scholar
  54. Hungria M, Andrade DDS, Chueire LMDO, Probanza A, Guttierrez-Mañero FJ, Meǵas M (2000) Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biol Biochem 32:1515–1528CrossRefGoogle Scholar
  55. Hynes MF, McGregor NF (1990) Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 4:567–574PubMedCrossRefGoogle Scholar
  56. Ilyin VK, Smirnov IA, Soldatov PE, Korniushenkova IN, Grinin AS, Lykov IN, Safronova SA (2004) Microbial utilisation of natural organic wastes. Acta Astronaut 54:357–361PubMedCrossRefGoogle Scholar
  57. Im W, Yokota A, Kim M, Lee S (2004) Kaistia adipata gen. nov., sp. nov., a novel α-proteobacterium. J Gen Appl Microbiol 50:249–254PubMedCrossRefGoogle Scholar
  58. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633PubMedCentralPubMedCrossRefGoogle Scholar
  59. Jordan DC (1984) Family III. Rhizobiaceae Conn 1938. In: Krieg N, Holt RG (eds) Bergey’s manual of systematic bacteriology, vol 1, 1st edn. The Williams and Wilkins, Baltimore, pp 234–235Google Scholar
  60. Judicial Commission of the International Committee on Systematics of Prokaryotes (2008) The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name‘Sinorhizobium adhaerens’ is not validly published. Opinion 84. Int J Syst Evol Microbiol 58:1973. doi:10.1099/ijs.0.2008/005991-0CrossRefGoogle Scholar
  61. Kampfer P, Neef A, Salkinoja-Salonen MS, Busse H (2002) Chelatobacter heintzii (Auling et al. 1993) is a later subjective synonym of Aminobacter aminovorans (Urakami et al. 1992). Int J Syst Evol Microbiol 52:835–839PubMedGoogle Scholar
  62. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338PubMedCrossRefGoogle Scholar
  63. Kosenko LV, Khailova GF, Korelov VE (2001) Fiziology biokhim. Kul's Rast 33:347–354Google Scholar
  64. Kim SJ, Weon HY, Kim YS, Anandham R, Yoo SH, Park IC, Kwon SW (2010) Kaistia terrae sp. nov., isolated from a wetland in Korea. Int J Syst Evol Microbiol 60:949–952PubMedCrossRefGoogle Scholar
  65. Kirichenko EV, Titova LV, Ya-Kots S (2004) The significance of exometabolites in the formation and operation of soybean-Rhizobium symbiosis. Appl Biochem Microbiol 40(5):490–493CrossRefGoogle Scholar
  66. Kiyokawa K, Yamamoto S, Sakuma K, Tanaka K, Moriguchi K, Suzuki K (2009) Construction of disarmed Ti plasmids transferable between Escherichia coli and Agrobacterium species. Appl Environ Microbiol 75:1845–1851PubMedCentralPubMedCrossRefGoogle Scholar
  67. Kumar A, Bhawsar NG, Badnagre P, Panse U, Gayakwad SR, Khasdeo K (2013) Isolation of Agrobacterium tumefaciens from soil and Optimization of Genomic & Plasmid DNA Extraction. Int J Adv Res 1:1–4Google Scholar
  68. Kuykendall LD (2005) Family I. Rhizobiaceae Conn 1938, 321AL. In: Brenner DJ, Krieg NR, Stanley JT (eds) Bergey’s manual of systematic bacteriology, vol 2. Springer, New York, pp 324–361Google Scholar
  69. Lee HW, Yu HS, Liu Q, Jung HM, An DS, Im WT, Jin FX, Lee ST (2007) Kaistia granuli sp. nov., isolated from anaerobic granules in an up flow anaerobic sludge blanket reactor. Int J Syst Evol Microbiol 57:2280–2283PubMedCrossRefGoogle Scholar
  70. Lee M, Woo SG, Ten LN (2011) Shinella daejeonensis sp. nov., a nitrate-reducing bacterium isolated from sludge of a leachate treatment plant. Int J Syst Evol Microbiol 61:2123–2128PubMedCrossRefGoogle Scholar
  71. Lin DX, Wang ET, Tang H, Han TX, He YR, Guan SH, Chen WX (2008) Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int J Syst Evol Microbiol 58:1409–1413PubMedCrossRefGoogle Scholar
  72. Lindström K, Martinez-Romero ME (2002) International committee on systematics of prokaryotes subcommittee on the taxonomy of Agrobacterium and Rhizobium. Int J Syst Evol Microbiol 52:2337CrossRefGoogle Scholar
  73. Lindström K, Murwira M, WillemS A, Altier N (2010) The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Res Microbiol 161:453–463PubMedCrossRefGoogle Scholar
  74. Lodwig E, Poole P (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22:37–78CrossRefGoogle Scholar
  75. Lodwig EM, Hosie AH, Bourdès A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422:722–726PubMedCrossRefGoogle Scholar
  76. López-Guerrero MG, Ormeño-Orrillo E, Acosta JL, Mendoza-Vargas A, Rogel MA, Ramírez MA, Rosenblueth M, Martínez-Romero J, Martínez-Romero E (2012) Rhizobial extrachromosomal replicon variability, stability and expression in natural niches. Plasmid 68:149–158PubMedCrossRefGoogle Scholar
  77. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  78. Marcondes J, Hansen E (2008) Transgenic lettuce seedlings carrying hepatitis B virus antigen HBsAg Braz. J Infect Dis 12:469–471Google Scholar
  79. Martínez-Romero E (2009) Coevolution in Rhizobium-legume symbiosis? DNA Cell Biol 28:361–370PubMedCrossRefGoogle Scholar
  80. Masson-Boivin C, Perret EGX, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466PubMedCrossRefGoogle Scholar
  81. Matsui T, Hirasawa K, Konishi J, Tanaka Y, Maruhashi K, Kurane R (2001) Microbial desulfurization of alkylated dibenzothiophene and alkylated benzothiophene by recombinant Rhodococcus sp. strain T09. Appl Microbiol Biotechnol 56:196–200PubMedCrossRefGoogle Scholar
  82. Matsui T, Shinzato N, Tamaki H, Muramatsu M, Hanada S (2009) Shinella yambaruensis sp. nov., a 3-methyl-sulfolane-assimilating bacterium isolated from soil. Int J Syst Evol Microbiol 59:536–539PubMedCrossRefGoogle Scholar
  83. Matthysse AG (2006) The genus Agrobacterium. In: The prokaryotes. Springer, New York, pp 91–114Google Scholar
  84. Maury S, Delaunay A, Mesnard F, Crônier D, Chabbert B, Geoffroy P, Legrand M (2010) O-methyltransferase(s)-suppressed plants produce lower amounts of phenolic vir inducers and are less susceptible to Agrobacterium tumefaciens infection. Planta 232:975–986PubMedCrossRefGoogle Scholar
  85. Mergaert J, Swings J (2006) Family IV. Phyllobacteriaceae fam. nov. In: List of new names and new combinations previously effectively, but not validly published, validation list no 107. Int J Syst Evol Microbio 56:1–6Google Scholar
  86. Meyer O, Stackebrandt E, Auling G (1993) Reclassification of ubiquinone Q-10 containing carboxidotrophic bacteria: transfer of [Pseudomonas] carboxydovorans” OM5T to Oligotropha, gen. nov., as Oligotropha carboxidovorans, comb. nov., transfer of [Alcaligenes] carboxydus” DSM 1086 T to Carbophilus, gen. nov., as Carbophilus carboxidus, comb. nov., transfer of [Pseudomonas] compransoris” DSM 1231 T to Zavarzinia, gen. nov., as Zavarzinia compransoris, comb. nov., and amended descriptions of the new genera. Syst Appl Microbiol 16:390–395CrossRefGoogle Scholar
  87. Meyer OO (2005) Genus IV Carbophilus. In: Brenner DJ, Krieg NR, Staley J (eds) Bergey's manual of systematic bacteriology, volume two the proteobacteria, part C the alpha-, beta-, delta-, and epsilonproteobacteria. Springer, New York, pp 346–347CrossRefGoogle Scholar
  88. Mnasri B, Saïdi S, Chihaoui SA, Mhamdi R (2012) Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Syst Appl Microbiol 35:263–269PubMedCrossRefGoogle Scholar
  89. Moffet ML, Colwell RR (1968) Adansonian analysis of the Rhizobiaceae. J Gen Microbiol 51:245–266CrossRefGoogle Scholar
  90. Mohamad OA, Hao X, Xie P, Hatab S, Lin Y, Wei G (2012) Biosorption of copper (II) from aqueous solution using non-living Mesorhizobium amorphae strain CCNWGS0123. Microbes Environ 27:234–241PubMedCentralPubMedCrossRefGoogle Scholar
  91. Moreira F, Gillis M, Pot B, Kersters K, Franco AA (1993) Characterization of rhizobia isolated from different divergence groups of tropical Leguminosae by comparative polyacrylamide gel electrophoresis of their total proteins. Syst Appl Microbiol 16:135–146CrossRefGoogle Scholar
  92. Moreira FMS, Siqueira JO (2006) Fixação Biológica de Nitrogênio Atmosférico. In: Microbiologia e bioquímica do solo. UFLA, Lavras, 488pGoogle Scholar
  93. Murto M, Björnsson L, Mattiasson B (2004) Impact of food industrial wase on anaerobic co-digestion of sewage sludge and pig manure. J Environ Manage 70:101–107PubMedCrossRefGoogle Scholar
  94. Norris DO (1965) Acid production by Rhizobium a unifying concept. Plant Soil 22(2):143–166CrossRefGoogle Scholar
  95. Notification List IJSEM (2002) Int J Syst Evol Microbiol 52:1077–1079CrossRefGoogle Scholar
  96. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedCrossRefGoogle Scholar
  97. Olivares J, Bedmar EJ, Sanjuán J (2013) Biological nitrogen fixation in the context of global change. MPMI 26:486–494PubMedCrossRefGoogle Scholar
  98. Paganelli FL, Lemos EGM, Carareto Alves LM (2011) Polyhydroxybutyrate in Rhizobium and Bradyrhizobium: quantification and phbC gene expression. World J Microbiol Biotechnol 27:773–778CrossRefGoogle Scholar
  99. Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC (2012) The Genomes OnLine Database (GOLD) v. 4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 40:D571–D579PubMedCentralPubMedCrossRefGoogle Scholar
  100. Parte AC (2014) LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42(Database issue):D613–D616Google Scholar
  101. Peter J, Young W, Haukka KE (1996) Diversity and phylogeny of rhizobia. New Phytol 133:87–94CrossRefGoogle Scholar
  102. Pinto FGS, Hungria M, Mercante FM (2007) Polyphasic characterization of Brazilian Rhizobium tropici strains effective in fixing N2 with common bean (Phaseolus vulgaris L.). Soil Biol Biochem 39:1851–1864CrossRefGoogle Scholar
  103. Pitzschke A (2013) Agrobacterium infection and plant defense-transformation success hangs by a thread. Front Plant Sci 18:519Google Scholar
  104. Provorov NA, Vorobyov NI (2008) Equilibrium between the “genuine mutualists” and “symbiotic cheaters” in the bacterial population co-evolving with plants in a facultative symbiosis. Theor Popul Biol 74:345–355PubMedCrossRefGoogle Scholar
  105. Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. MPMI 12:293–318PubMedCrossRefGoogle Scholar
  106. Puławska J, Willems A, Sobiczewski P (2006) Rapid and specific identification of four Agrobacterium species and biovars using multiplex PCR. Syst Appl Microbiol 29:470–479PubMedCrossRefGoogle Scholar
  107. Rees DC, Howard JB (2000) Nitrogenase: standing at the crossroads. Curr Opin Chem Biol 4:559–566PubMedCrossRefGoogle Scholar
  108. Reeve W, Chain P, O’Hara G, Ardley J, Nandesena K, Bräu L, Tiwari R, Malfatti S, Kiss H, Lapidus A, Co-peland A, Nolan M, Land M, Hauser L, Chang Y, Ivanova N, Mavromatis K, Markowitz V, Kyrpides N, Gollagher M, Yates R, Dilworth M, Howieson J (2010) Complete genome sequence of the Medicago microsym-biont Ensifer (Sinorhizobium) medicae strain WSM419. Stand Genomic Sci 2:77–86PubMedCentralPubMedCrossRefGoogle Scholar
  109. Renalier MH, Batut J, Ghai JYOTSNA, Terzaghi B, Gherardi M, David M, Vasse J, Trughet G, Huguet T (1987) A new symbiotic cluster on the pSym megaplasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J Bacteriol 169:2231–2238PubMedCentralPubMedGoogle Scholar
  110. Rendueles O, Kaplan JB, Ghigo JM (2013) Antibiofilm polysaccharides. Environ Microbiol 15:334–346PubMedCentralPubMedCrossRefGoogle Scholar
  111. Ribeiro RA, Barcellos FG, Thompson FL, Hungria M (2009) Multilocus sequence analysis of Brazilian Rhizobium microsymbionts of common bean (Phaseolus vulgaris L.) reveals unexpected taxonomic diversity. Res Microbiol 160:297–306PubMedCrossRefGoogle Scholar
  112. Rousseaux S, Soulas G, Hartman A (2002) Plasmid localisation of atrazine-degrading genes in newly described Chelatobacter and Arthrobacter strains FEMS. Microbiol Ecol 41:69–75CrossRefGoogle Scholar
  113. Sathiyanarayanan G, Kiran GS, Selvin J (2013) Synthesis of silver nanoparticles by polysaccharide bioflocculant produced from marine Bacillus subtilis MSBN17. Colloids Surf B 102:13–20CrossRefGoogle Scholar
  114. Scholla MH, Elkan GH (1984) Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans. Int J Syst Bacteriol 34(4):484–486CrossRefGoogle Scholar
  115. Schroth MN, Thompson JP, Hildebrand DC (1965) Isolation os Agrobacterium tumefaciens-A. radiobacter group from soil. Phytopathology 55:645–647Google Scholar
  116. Shah AA, Hasan F, Hameed A, Ahmed S (2008) Biological degradation of plastics: a comprehensive review. Biotechnol Adv 26:246–265PubMedCrossRefGoogle Scholar
  117. Shams M, Vial L, Chapulliot D, Nesme X, Lavire C (2013) Rapid and accurate species and genomic species identification and exhaustive population diversity assessment of Agrobacterium spp. using recA-based PCR. Syst Appl Microbiol 36:351–358PubMedCrossRefGoogle Scholar
  118. Sheng J, Citovsky V (1996) Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8:1699PubMedCentralPubMedCrossRefGoogle Scholar
  119. Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 5:7PubMedCentralPubMedCrossRefGoogle Scholar
  120. Slater SC, Goldman BS, Goodner B, Setubal JC, Farrand SK, Nester EW, Burr TJ, Banta L, Dickerman AW, Paulsen I, Otten L, Suen G, Welch R, Almeida NF, Arnold F, Burton OT, Du Z, Ewing A, Godsy E, Heisel S, Houmiel KL, Jhaveri J, Lu J, Miller NM, Norton S, Chen Q, Phoolcharoen W, Ohlin V, Ondrusek D, Pride N, Stricklin SL, Sun J, Wheeler C, Wilson L, Zhu H, Wood DW (2009) Genome sequences of three agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J Bacteriol 191(8):2501–2511PubMedCentralPubMedCrossRefGoogle Scholar
  121. Smith EF, Townsend CO (1907) A plant-tumor of bacterial origin. Science 25:671–673PubMedCrossRefGoogle Scholar
  122. Somasegaran P, Hoben HJ (1994) Handbook for rhizobia: methods in legume-Rhizobium technology. Springer, New YorkCrossRefGoogle Scholar
  123. Sutherland IW (1998) Novel and established applications of microbial polysaccharides. Trends Biotechnol 16:41–46PubMedCrossRefGoogle Scholar
  124. Sutherland IW (2001) Microbial polysaccharides from Gram-negative bacteria. Int Dairy J 11:663–674CrossRefGoogle Scholar
  125. Thies JE, Holmes EM, Vachot A (2001) Application of molecular techniques to studies in Rhizobium ecology: a review. Anim Prod Sci 41:299–319CrossRefGoogle Scholar
  126. Tibayrenc M (2009) Multilocus enzyme electrophoresis for parasites and other pathogens. Methods Mol Biol 551:13–25PubMedCrossRefGoogle Scholar
  127. Tighe SW, de Lajudie P, Dipietro K, Lindstrom K, Nick G, Jarvis BD (2000) Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int J Syst Evol Microbiol 50:787–801PubMedCrossRefGoogle Scholar
  128. Tindall BJ (2008) The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘Sinorhizobium adhaerens’ is not validly published. Opinion 84. Int J Syst Evol Microbiol 58:1973CrossRefGoogle Scholar
  129. Tzfira T, Citovsky V (2000) From host recognition to T‐DNA integration: the function of bacterial and plant genes in the Agrobacterium-plant cell interaction. Mol Plant Pathol 1:201–212PubMedCrossRefGoogle Scholar
  130. Tzfira T, Citovsky V (2006) Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 17:147–154PubMedCrossRefGoogle Scholar
  131. Valentine AJ, Benedito VA, Kang Y (2010) Legume nitrogen fixation and soil abiotic stress: from physiology to genomics and beyond. Ann Plant Rev 42:207–248CrossRefGoogle Scholar
  132. Valvekens D, Van Montagu M, Van Lijsebettens M (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci 85:5536–5540PubMedCentralPubMedCrossRefGoogle Scholar
  133. van Berkum P, Beyene D, Eardly BD (1996) Phylogenetic relationships among Rhizobium species nodulating the common bean (Phaseolus vulgaris L.). Int J Syst Bacteriol 46:240–244PubMedCrossRefGoogle Scholar
  134. Van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD (1998) Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Bacteriol 48(1):13–22PubMedCrossRefGoogle Scholar
  135. Van Rhijn P, Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59(1):124–142PubMedCentralPubMedGoogle Scholar
  136. Vandamme P, Pot B, Gillis M, De Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438PubMedCentralPubMedGoogle Scholar
  137. Varani AM, Monteiro-Vitorello CB, Nakaya HI, Van Sluys MA (2013) The role of prophage in plant-pathogenic bacteria. Annu Rev Phytopathol 51:429–451PubMedCrossRefGoogle Scholar
  138. Vaz-Moreira I, Faria C, Lopes AR, Svensson LA, Moore ER, Nunes OC, Manaia CM (2010) Shinella fusca sp. nov., isolated from domestic waste compost. Int J Syst Evol Microbiol 60:144–148PubMedCrossRefGoogle Scholar
  139. Vincent JM (1970) Manual for the practical study of root nodule bacteria. International biological programme handbook, vol 15. Blackwell Scientific Publications, Oxford, p 164Google Scholar
  140. Vincent JM, Humphrey B (1970) Taxonomically significant group antigens in Rhizobium. J Gen Microbiol 63:379–382PubMedCrossRefGoogle Scholar
  141. Wang Y, Ahmed Z, Feng W, Li C, Song S (2008) Physicochemical properties of exopolysaccharide produced by Lactobacillus kefiranofaciens ZW3 isolated from Tibet kefir. Int J Biol Macromol 43:283–288PubMedCrossRefGoogle Scholar
  142. Weber CF, King GM (2010) Distribution and diversity of carbon monoxide‐oxidizing bacteria and bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit. Environ Microbiol 12:1855–1867PubMedCrossRefGoogle Scholar
  143. Whitfield C (1988) Bacterial extracellular polysaccharides. Can J Microbiol 34:415–420PubMedCrossRefGoogle Scholar
  144. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14CrossRefGoogle Scholar
  145. Willems A, Fernández-López M, Muñoz-Adelantado E, Goris J, De Vos P, Martínez-Romero E, Toro N, Gillis M (2003) Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an opinion. Int J Syst Evol Microbiol 53:1207–1217PubMedCrossRefGoogle Scholar
  146. Wise AA, Fang F, Lin YH, He F, Lynn DG, Binns AN (2010) The receiver domain of hybrid histidine kinase VirA: an enhancing factor for vir gene expression in Agrobacterium tumefaciens. J Bacteriol 192:1534–1542PubMedCentralPubMedCrossRefGoogle Scholar
  147. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Jr Almeida NF, Woo L, Chen Y, Paulsen IT, Eisen JA, Karp PD, Sr Bovee D, Chapman P, Clendenning J, Deatherage G, Gillet W, Grant C, Kutyavin T, Levy R, Li MJ, McClelland E, Palmieri A, Raymond C, Rouse G, Saenphimmachak C, Wu Z, Romero P, Gordon D, Zhang S, Yoo H, Tao Y, Biddle P, Jung M, Krespan W, Perry M, Gordon-Kamm B, Liao L, Kim S, Hendrick C, Zhao ZY, Dolan M, Chumley F, Tingey SV, Tomb JF, Gordon MP, Olson MV, Nester EW (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317–2323PubMedCrossRefGoogle Scholar
  148. Wu G, Kang HB, Zhang XY, Shao HB, Chu LY, Ruan CJ (2010) A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. J Hazard Mater 174:1–8PubMedCrossRefGoogle Scholar
  149. Xie P, Hao X, Mohamad OA, Liang J, Wei G (2013) Comparative study of chromium biosorption by Mesorhizobium amorphae strain CCNWGS0123 in single and binary mixtures. Appl Biochem Biotechnol 169:570–587PubMedCrossRefGoogle Scholar
  150. Yamaguchi H, Tanaka H, Hasegawa M, Tokuda M, Asami T, Suzuki Y (2012) Phytohormones and willow gall induction by a gall-inducing sawfly. New Phytol 196:586–595PubMedCrossRefGoogle Scholar
  151. Young JM (2010) Sinorhizobium versus Ensifer: may a taxonomy subcommittee of the ICSP contradict the Judicial Commission? Int J Syst Evol Microbiol 60:1711–1713PubMedCrossRefGoogle Scholar
  152. Young P (2013) From Rhizobium to Sinorhizobium, from Sinorhizobium to Ensifer? Rhizobium—writing about bacteria and their genomes.
  153. Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF (1978) A proposed nomenclature and classification for plant pathogenic bacteria. N Z J Agric Res 21:153–177CrossRefGoogle Scholar
  154. Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicolaand R. vitis. Int J Syst Evol Microbiol 51:89–103PubMedCrossRefGoogle Scholar
  155. Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2003) Classification and nomenclature of Agrobacterium and Rhizobium—a reply to Farrand et al. (2003). Int J Syst Evol Microbiol 53:1689–1695PubMedCrossRefGoogle Scholar
  156. Young JM, Kerr A, Sawada H (2005) Genus II. Agrobacterium Conn 1942, 359AL. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey's manual of systematic bacteriology, volume two the proteobacteria, part C the alpha-, beta-, delta-, and epsilonproteobacteria. Springer, New York, pp 340–345CrossRefGoogle Scholar
  157. Young JP, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS, Mauchline TH, East AK, Quail MA, Churcher C, Arrowsmith C, Cherevach I, Chillingworth T, Clarke K, Cronin A, Davis P, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, Whitehead S, Parkhill J (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34PubMedCentralPubMedCrossRefGoogle Scholar
  158. Yuan Z, Van Briesen JM (2006) The formation of intermediates in EDTA and NTA biodegradation. Environ Eng Sci 23:533–544CrossRefGoogle Scholar
  159. Yutani M, Taniguchi H, Borjihan H, Ogita A,Fujita K, Tanaka T (2011) Alliinase from Ensifer adhaerens and its use for generation of fungicidal activity. AMB Express 1:2.
  160. Zakhia F, De Lajudie P (2001) Taxonomy of rhizobia. Agronomie 21:569–576CrossRefGoogle Scholar
  161. Zambryski P, Joos H, Genetello C, Leemans J, Van Montagu M, Schell J (1983) Ti plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity. EMBO J 2:2143PubMedCentralPubMedGoogle Scholar
  162. Zeph LR (1986) Indirect phage analysis studies of the activity of nonobligate predator bacteria in soil. Thesis, Pennsylvania State University Park, PennsylvaniaGoogle Scholar
  163. Zeph LR, Casida LE (1986) Gram-negative versus gram-positive (actinomycete) bacterial predators of bacteria in soil. Appl Environ Microbiol 52:2319–2823Google Scholar
  164. Zhou GC, Wang Y, Zhai S, Ge F, Liu ZH, Dai YJ, Yuan S, Hou JY (2013) Biodegradation of the neonicotinoid insecticide thiamethoxam by the nitrogen-fixing and plant-growth-promoting rhizobacterium Ensifer adhaerens strain TMX-23. Appl Microbiol Biotechnol 97(9):4065–4074. doi: 10.1007/s00253-012-4638-3. Epub 2012 Dec 30Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lucia Maria Carareto Alves
    • 1
  • Jackson Antônio Marcondes de Souza
    • 2
  • Alessandro de Mello Varani
    • 1
  • Eliana Gertrudes de Macedo Lemos
    • 1
  1. 1.Departamento de TecnologiaUniversidade Estadual PaulistaSão PauloBrazil
  2. 2.Departamento de Biologia Aplicada à AgropecuáriaUniversidade Estadual PaulistaSão PauloBrazil

Personalised recommendations