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Antibiotics Resistance in Rhizobium: Type, Process, Mechanism and Benefit for Agriculture

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Abstract

The use of high-quality rhizobial inoculants on agricultural legumes has contributed substantially to the N economy of farming systems through inputs from biological nitrogen fixation (BNF). Large populations of symbiotically effective rhizobia should be available in the rhizosphere for symbiotic BNF with host plants. The rhizobial populations should also be able to compete and infect host plants. However, the rhizosphere comprises large populations of different microorganisms. Some of these microorganisms naturally produce antibiotics which are lethal to susceptible rhizobial populations in the soil. Therefore, intrinsic resistance to antibiotics is a desirable trait for the rhizobial population. It increases the rhizobia’s chances of growth, multiplication and persistence in the soil. With a large population of rhizobia in the soil, infectivity of host plants and the subsequent BNF efficiency can be guaranteed. This review, therefore, puts together findings by various researchers on antibiotic resistance in bacteria with the main emphasis on rhizobia. It describes the different modes of action of different antibiotics, the types of antibiotic resistance exhibited by rhizobia, the mechanisms of acquisition of antibiotic resistance in rhizobia and the levels of tolerance of different rhizobial species to different antibiotics.

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References

  1. Abaidoo R, Keyser H, Singleton P, Borthakur D (2002) Comparison of molecular and antibiotic resistance profile methods for the population analysis of Bradyrhizobium spp. (TGx) isolates that nodulate the new TGx soybean cultivars in Africa. J Appl Microbiol 92:109–117

    Article  CAS  PubMed  Google Scholar 

  2. Alekshun MN, Levy SB (2007) Molecular mechanisms of antibacterial multidrug resistance. Cell 128:1037–1050

    Article  CAS  PubMed  Google Scholar 

  3. Alexandre A, Laranjo M, Oliveira S (2006) Natural populations of chickpea rhizobia evaluated by antibiotic resistance profiles and molecular methods. Microb Ecol 51:128–136

    Article  CAS  PubMed  Google Scholar 

  4. Alexandre A, Oliveira S (2011) Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. FEMS Microbiol Ecol 75:28–36

    Article  CAS  PubMed  Google Scholar 

  5. Anand A, Jaiswal SK, Dhar B, Vaishampayan A (2012) Surviving and thriving in terms of symbiotic performance of antibiotic and phage-resistant mutants of Bradyrhizobium of soybean [Glycine max (L.) Merrill]. Curr Microbiol 65:390–397

    Article  CAS  PubMed  Google Scholar 

  6. Andes D, Craig W (2005) Cephalosporins. In: Mandell GL, Bennett JE, Dolin R (eds) Principles and Practice of Infectious Diseases, 6. baskı’’kitabında s. Elsevier Churchill Livingstone, Philadelphia, pp 294–311

    Google Scholar 

  7. Arredondo-Peter R, Escamilla E (1993) Sodium dodecyl sulfate-polyacrylamide gel electrophoresis protein banding patterns among Rhizobium leguminosarum biovar phaseoli strains isolated from the Mexican bean Phaseolus coccineus. Appl Environ Microbiol 59:3960–3962

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Aune TEV, Aachmann FL (2010) Methodologies to increase the transformation efficiencies and the range of bacteria that can be transformed. Appl Microbiol Biotechnol 85:1301–1313

    Article  CAS  PubMed  Google Scholar 

  9. Ausili P, Borisov A, Lindblad P, Mårtensson A (2002) Cadmium affects the interaction between peas and root nodule bacteria. Acta Agric Scand Sect B Plant Soil Sci 52:8–17

    CAS  Google Scholar 

  10. Baba T, Schneewind O (1998) Instruments of microbial warfare: bacteriocin synthesis, toxicity and immunity. Trends Microbiol 6:66–71

    Article  CAS  PubMed  Google Scholar 

  11. Bader MW, Navarre WW, Shiau W, Nikaido H, Frye JG, McClelland M, Fang FC, Miller SI (2003) Regulation of Salmonela typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol 50:219–230

    Article  CAS  PubMed  Google Scholar 

  12. Balassa G (1963) Genetic transformation of Rhizobium: A review of the work of R. Balassa. Bacteriol Rev 27:228

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Belachew T (2010) Intrinsic antibiotic resistance, survival of Rhizobium leguminosarum strains and fixation potential of pea varieties (Pisum sativum L.) in southeast Ethiopia. Int J Microbiol Res 2:75–79

    Google Scholar 

  14. Ben W, Qiang Z, Adams C, Zhang H, Chen L (2008) Simultaneous determination of sulfonamides, tetracyclines and tiamulin in swine wastewater by solid-phase extraction and liquid chromatography–mass spectrometry. J Chromatogr 1202:173–180

    Article  CAS  Google Scholar 

  15. Berge O, Lodhi A, Brandelet G, Santaella C, Roncato M-A, Christen R, Heulin T, Achouak W (2009) Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol 59:367–372

    Article  CAS  PubMed  Google Scholar 

  16. Beringer J (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198

    CAS  PubMed  Google Scholar 

  17. Beynon J, Josey D (1980) Demonstration of heterogeneity in a natural population of Rhizobium phaseoli using variation in intrinsic antibiotic resistance. J Gen Microbiol 118:437–442

    Google Scholar 

  18. Bibi F, Chung EJ, Khan A, Jeon CO, Chung YR (2012) Rhizobium halophytocola sp. nov., isolated from the root of a coastal dune plant. Int J Syst Evol Microbiol 62:1997–2003

    Article  CAS  PubMed  Google Scholar 

  19. Botha WJ, Jaftha JB, Bloem JF, Habig JH, Law IJ (2004) Effect of soil bradyrhizobia on the success of soybean inoculant strain CB 1809. Microbiol Res 159:219–231

    Article  CAS  PubMed  Google Scholar 

  20. Brígido C, Oliveira S (2013) Most acid-tolerant chickpea mesorhizobia show induction of major chaperone genes upon acid shock. Microb Ecol 65:145–153

    Article  PubMed  CAS  Google Scholar 

  21. Brockman F, Bezdicek D (1989) Diversity within serogroups of Rhizobium leguminosarum biovar viceae in the Palouse region of eastern Washington as indicated by plasmid profiles, intrinsic antibiotic resistance, and topography. Appl Environ Microbiol 55:109–115

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Bromfield E, Lewis D, Barran L (1985) Cryptic plasmid and rifampin resistance in Rhizobium meliloti influencing nodulation competitiveness. J Bacteriol 164:410–413

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Calvori C, Frontali L, Leoni L, Tecce G (1965) Effect of rifamycin on protein synthesis. Nature 207:417–418

    Article  CAS  PubMed  Google Scholar 

  24. Carpenter CF, Chambers HF (2004) Daptomycin: another novel agent for treating infections due to drug-resistant gram-positive pathogens. Clin Infect Dis 38:994–1000

    Article  CAS  PubMed  Google Scholar 

  25. Chahboune R, Carro L, Peix A, Barrijal S, Velázquez E, Bedmar EJ (2011) Bradyrhizobium cytisi sp. nov. isolated from effective nodules of Cytisus villosus in Morocco. Int J Syst Evol Microbiol 61:2922–2927

    Article  PubMed  Google Scholar 

  26. Chahboune R, Carro L, Peix A, Ramírez-Bahena M-H, Barrijal S, Velázquez E, Bedmar EJ (2012) Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst Appl Microbiol 35:302–305

    Article  CAS  PubMed  Google Scholar 

  27. Chang YL, Wang JY, Wang ET, Liu HC, Sui XH, Chen WX (2011) Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea. Int J Syst Evol Microbiol 61:2496–2502

    Article  PubMed  Google Scholar 

  28. Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cole MA, Elkan G (1979) Multiple antibiotic resistance in Rhizobium japonicum. Appl Environ Microbiol 37:867–870

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Cole MA, Elkan GH (1973) Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob Agents Chemother 4:248–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Courvalin P (2008) New plasmid-mediated resistances to antimicrobial agents. Arch Microbiol 189:289–291

    Article  CAS  PubMed  Google Scholar 

  32. Dadarwal K, Sindhu S, Garg R (1987) Effect of curing on genes controlling antibiotic resistance and symbiosis in cowpea misc. rhizobia. Ind J Micobiol 27:16–21

    CAS  Google Scholar 

  33. Dakora F, Keya S (1997) Contribution of legume nitrogen fixation to sustainable agriculture in Sub-Saharan Africa. Soil Biol Biochem 29:809–817

    Article  CAS  Google Scholar 

  34. Dall’Agnol RF, Ribeiro RA, Ormeño-Orrillo E, Rogel MA, Delamuta JRM, Andrade DS, Martínez-Romero E, Hungria M (2013) Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. Int J Syst Evol Microbiol 63:4167–4173

    Article  PubMed  Google Scholar 

  35. Date R, Hurse L (1991) Intrinsic antibiotic resistance and serological characterization of populations of indigenous Bradyrhizobium isolated from nodules of Desmodium intortum and Macroptilium atropurpureum in three soils of SE Queensland. Soil Biol Biochem 23:551–561

    Article  Google Scholar 

  36. Datta N, Hedges R (1972) Trimethoprim resistance conferred by W plasmids in Enterobacteriaceae. J Gen Microbiol 72:349–355

    Article  CAS  PubMed  Google Scholar 

  37. Datta N, Hedges R, Shaw EJ, Sykes R, Richmond M (1971) Properties of an R factor from Pseudomonas aeruginosa. J Bacteriol 108:1244–1249

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Davies J, Spiegelman GB, Yim G (2006) The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9:445–453

    Article  CAS  PubMed  Google Scholar 

  39. D’Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311:374–377

    Article  PubMed  Google Scholar 

  40. Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martínez-Romero E, Hungria M (2013) Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 63:3342–3351

    Article  CAS  PubMed  Google Scholar 

  41. Djedidi S, Yokoyama T, Ohkama-Ohtsu N, Risal CP, Abdelly C, Sekimoto H (2011) Stress tolerance and symbiotic and phylogenic features of root nodule bacteria associated with Medicago species in different bioclimatic regions of Tunisia. Microb Environ 26:36–45

    Article  Google Scholar 

  42. Doi Y, Wachino J-I, Arakawa Y (2008) Nomenclature of plasmid-mediated 16S rRNA methylases responsible for panaminoglycoside resistance. Antimicrob Agent Chemother 52:2287–2288

    Article  CAS  Google Scholar 

  43. Douthwaite S, Aagaard C (1993) Erythromycin binding is reduced in ribosomes with conformational alterations in the 23 S rRNA peptidyl transferase loop. J Mol Biol 232:725–731

    Article  CAS  PubMed  Google Scholar 

  44. Dowdle SF, Bohlool BB (1985) Predominance of fast-growing Rhizobium japonicum in a soybean field in the People’s Republic of China. Appl Environ Microbiol 50:1171–1176

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Drlica K, Malik M (2003) Fluoroquinolones: action and resistance. Curr Topic Medi Chem 3:249–282

    Article  CAS  Google Scholar 

  46. Drlica K, Zhao X (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61:377–392

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Durán D, Rey L, Mayo J, Zúñiga-Dávila D, Imperial J, Ruiz-Argüeso T, Martínez-Romero E, Ormeño-Orrillo E (2014) Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol 64:2072–2078

    Article  PubMed  Google Scholar 

  48. Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (2006) The prokaryotes: a handbook on the biology of bacteria: proteobacteria: ecophysiology, isolation, identification, applications. Springer, New York.

    Google Scholar 

  49. Eaglesham A, Elkan G (1987) The use of intrinsic antibiotic resistance for Rhizobium study. Symbiotic Nitrogen Fixat Technol 185–204

  50. Eliopoulos GM, Meka VG, Gold HS (2004) Antimicrobial resistance to linezolid. Clin Infect Dis 39:1010–1015

    Article  Google Scholar 

  51. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Frioni L, Rodrıguez A, Meerhoff M (2001) Differentiation of rhizobia isolated from native legume trees in Uruguay. Appl Soil Ecol 16:275–282

    Article  Google Scholar 

  53. Gadre S, Mazumdar L, Modi V, Parekh V (1967) Interspecific transformation in Rhizobium. Arch für Mikrobiologie 57:388–391

    Article  CAS  Google Scholar 

  54. Galimand M, Courvalin P, Lambert T (2003) Plasmid-mediated high-level resistance to aminoglycosides in Enterobacteriaceae due to 16S rRNA methylation. Antimicrob Agent Chemother 47:2565–2571

    Article  CAS  Google Scholar 

  55. Garg F, Beri N, Tauro P (1985) Intrinsic antibiotic resistance in chickpea (Cicer arietinum) rhizobia. The J Agricult Sci 105:85–89

    Article  CAS  Google Scholar 

  56. Gemell L, Roughley R (1993) Counting rifampicin-resistant rhizobia when a minor component of the soil rhizobial flora. Soil Biol Biochem 25:539–544

    Article  Google Scholar 

  57. Ghosh S, LaPara TM (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 1:191–203

    Article  CAS  PubMed  Google Scholar 

  58. Glynn P, Higgins P, Squartini A, O’Gara F (1985) Strain identification in Rhizobium trifolii using DNA restriction analysis, plasmid DNA profiles and intrinsic antibiotic resistances. FEMS Microbiol Lett 30:177–182

    Article  CAS  Google Scholar 

  59. Gonzalez-Pasayo R, Martinez-Rpmero E (2000) Multiresistance genes of Rhizobium etli CFN42. MPMI 13:572–577

    Article  CAS  PubMed  Google Scholar 

  60. Graham P (1963) Antibiotic sensitivities of root nodule bacteria, vol 16. CSIRO publishing, Collingwood, p 557

    Google Scholar 

  61. Gu CT, Wang ET, Tian CF, Han TX, Chen WF, Sui XH, Chen WX (2008) Rhizobium miluonense sp. nov., a symbiotic bacterium isolated from Lespedeza root nodules. Int J Syst Evol Microbiol 58:1364–1368

    Article  CAS  PubMed  Google Scholar 

  62. Guerrouj K, Ruíz-Díez B, Chahboune R, Ramírez-Bahena M-H, Abdelmoumen H, Quiñones MA, El Idrissi MM, Velázquez E, Fernández-Pascual M, Bedmar EJ (2013) Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol 36:218–223

    Article  CAS  PubMed  Google Scholar 

  63. Gupta B, Kleczkowska J (1962) A study of some mutations in a strain of Rhizobium trifolii. J Gen Microbiol 27:473–476

    Article  CAS  PubMed  Google Scholar 

  64. Hagedorn C (1979) Relationship of antibiotic resistance to effectiveness in Rhizobium trifolii populations. Soil Sci Soc Am J 43:921–925

    Article  CAS  Google Scholar 

  65. Han TX, Wang ET, Wu LJ, Chen WF, Gu JG, Gu CT, Tian CF, Chen WX (2008) Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China. Int J Syst Evol Microbiol 58:1693–1699

    Article  CAS  PubMed  Google Scholar 

  66. Hastings P, Rosenberg SM, Slack A (2004) Antibiotic-induced lateral transfer of antibiotic resistance. Trend Microbiol 12:401–404

    Article  CAS  Google Scholar 

  67. Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243

    Article  CAS  PubMed  Google Scholar 

  68. Heumann W, Pühler A, Wagner E (1971) The two transfer regions of the Rhizobium lupini conjugation. I. Fertility factor elimination and one way transfer. MGG 113:308–315

    Article  CAS  PubMed  Google Scholar 

  69. Heumann W, Pühler A, Wagner E (1973) The two transfer regions of the Rhizobium lupini conjugation. II. Genetic characterization of the transferred chromosomal segments. MGG 126:267–274

    Article  CAS  PubMed  Google Scholar 

  70. Hong W, Zeng J, Xie J (2014) Antibiotic drugs targeting bacterial RNAs. Acta Pharm Sin B 4:258–265

    Article  PubMed  PubMed Central  Google Scholar 

  71. Howie WJ, Suslow T (1991) Role of antibiotic biosynthesis in the inhibition of Pythium ultimoum in the cotton spermosphere and rhizosphere. Mol Plant Microbe Interact 4:393–399

    Article  CAS  Google Scholar 

  72. Islam MS, Kawasaki H, Muramatsu Y, Nakagawa Y, Seki T (2008) Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci Biotech Biochem 72:1416–1429

    Article  CAS  Google Scholar 

  73. Jenkins M, Bottomley P (1985) Composition and field distribution of the population of Rhizobium meliloti in root nodules of uninoculated field-grown alfalfa. Soil Biol Biochem 17:173–179

    Article  Google Scholar 

  74. Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 235:178–185

    Article  PubMed  CAS  Google Scholar 

  75. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15:475–479

    Article  CAS  PubMed  Google Scholar 

  76. Karcı A, Balcıoğlu IA (2009) Investigation of the tetracycline, sulfonamide, and fluoroquinolone antimicrobial compounds in animal manure and agricultural soils in Turkey. Sci Total Environ 407:4652–4664

    Article  PubMed  CAS  Google Scholar 

  77. King G, Murray NE (1994) Restriction enzymes in cells, not eppendorfs. Trend Microbiol 2:465–469

    Article  CAS  Google Scholar 

  78. Kingsley MT, Bohlool BB (1983) Characterization of Rhizobium sp. (Cicer arietinum L.) by immunofluorescence, immunodiffusion, and intrinsic antibiotic resistance. Can J Microbiol 29:518–526

    Article  Google Scholar 

  79. Kittiwongwattana C, Thawai C (2014) Rhizobium lemnae sp. nov., a bacterial endophyte of Lemna aequinoctialis. Int J Syst Evol Microbiol 64:2455–2460

    Article  CAS  PubMed  Google Scholar 

  80. Knapp CW, Dolfing J, Ehlert PA, Graham DW (2009) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Tech 44:580–587

    Article  CAS  Google Scholar 

  81. Kobayashi G (1980) Actinomycetoma: the fungus-like bacteria. Microbiology Harper and Row, Philadelphia, pp 298–321

    Google Scholar 

  82. Kobayashi N, Nishino K, Yamaguchi A (2001) Novel Macrolide-specific ABC-type efflux transporter in Escherichia coli. J Bacteriol 183:5639–5644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Kotra L, Mobashery S (1998) β-Lactam antibiotics, β-lactamases and bacterial resistance. Bull de l’Inst Pasteur 96:139–150

    Article  CAS  Google Scholar 

  84. Kowalski M (1971) Transduction in Rhizobium meliloti. Plant Soil 35:63–66

    Article  Google Scholar 

  85. Kroiss J, Kaltenpoth M, Schneider B, Schwinger M-G, Hertweck C, Maddula RK, Strohm E, Svatoš A (2010) Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 6:261–263

    Article  CAS  PubMed  Google Scholar 

  86. Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10:597–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Kumbhar C, Watve M (2013) Why antibiotics: A comparative evaluation of different hypotheses for the natural role of antibiotics and an evolutionary synthesis

  88. Kuykendall L (1979) Transfer of R factors to and between genetically marked sublines of Rhizobium japonicum. Appl Environ Microbiol 37:862–866

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10:S122–S129

    Article  CAS  PubMed  Google Scholar 

  90. Li D-M, Alexander M (1988) Co-inoculation with antibiotic-producing bacteria to increase colonization and nodulation by rhizobia. Plant Soil 108:211–219

    Article  Google Scholar 

  91. Lin DX, Chen WF, Wang FQ, Hu D, Wang ET, Sui XH, Chen WX (2009) Rhizobium mesosinicum sp. nov., isolated from root nodules of three different legumes. Int J Syst Evol Microbiol 59:1919–1923

    Article  PubMed  Google Scholar 

  92. Linares J, Gustafsson I, Baquero F, Martinez J (2006) Antibiotics as intermicrobial signaling agents instead of weapons. Proc Nat Acad Sci 103:19484–19489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Liu TY, Li Y, Liu XX, Sui XH, Zhang XX, Wang ET, Chen WX, Chen WF, Puławska J (2012) Rhizobium cauense sp. nov., isolated from root nodules of the herbaceous legume Kummerowia stipulacea grown in campus lawn soil. Syst Appl Microbiol 35:415–420

    Article  CAS  PubMed  Google Scholar 

  94. Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Lu JK, Dou YJ, Zhu YJ, Wang SK, Sui XH, Kang LH (2014) Bradyrhizobium ganzhouense sp. nov., an effective symbiotic bacterium isolated from Acacia melanoxylon R. Br. nodules. Int J Syst Evol Microbiol 64:1900–1905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Lu YL, Chen WF, Han LL, Wang ET, Chen WX (2009) Rhizobium alkalisoli sp. nov., isolated from Caragana intermedia growing in saline-alkaline soils in the north of China. Int J Syst Evol Microbiol 59:3006–3011

    Article  CAS  Google Scholar 

  97. Maiden MC (1998) Horizontal genetic exchange, evolution, and spread of antibiotic resistance in bacteria. Clinic Infect Dis 27:S12–S20

    Article  CAS  Google Scholar 

  98. Marger MD, Saier MH (1993) A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trend Biochem Sci 18:13–20

    Article  CAS  PubMed  Google Scholar 

  99. Mc Dermott PF, Walker RD, White DG (2003) Antimicrobials: modes of action and mechanisms of resistance. Int J Toxicol 22:135–143

    Article  CAS  Google Scholar 

  100. McLaughlin W, Ahmad MH (1984) Intrinsic antibiotic resistance and streptomycin uptake in cowpea rhizobia. FEMS Microbiol Lett 21:299–303

    Article  CAS  Google Scholar 

  101. McManus MC (1997) Mechanisms of bacterial resistance to antimicrobial agents. Am J Health Syst Phar 54:1420–1433

    CAS  Google Scholar 

  102. Mehta R, Champney WS (2002) 30S ribosomal subunit assembly is a target for inhibition by aminoglycosides in Escherichia coli. Antimicrob Agent Chemother 46:1546–1549

    Article  CAS  Google Scholar 

  103. Meyer MC, Pueppke SG (1980) Differentiation of Rhizobium japonicum strain derivatives by antibiotic sensitivity patterns, lectin binding, and utilization of biochemicals. Can J Microbiol 26:606–612

    Article  CAS  PubMed  Google Scholar 

  104. Mingeot-Leclercq M-P, Glupczynski Y, Tulkens PM (1999) Aminoglycosides: activity and resistance. Antimicrob Agent Chemother 43:727–737

    CAS  Google Scholar 

  105. Mnasri B, Liu TY, Saidi S, Chen WF, Chen WX, Zhang XX, Mhamdi R (2014) Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 64:1501–1506

    Article  CAS  PubMed  Google Scholar 

  106. Mpepereki S, Makonese F, Wollum A (1997) Physiological characterization of indigenous rhizobia nodulating Vigna unguiculata in Zimbabwean soils. Symbiosis 22, Philadelphia

    Google Scholar 

  107. Mueller J, Skipper H, Shipe E, Grimes L, Wagner S (1988) Intrinsic antibiotic resistance in Bradyrhizobium japonicum. Soil Biol Biochem 20:879–882

    Article  CAS  Google Scholar 

  108. Mukhtar TA, Koteva KP, Hughes DW, Wright GD (2001) Vgb from Staphylococcus aureus inactivates streptogramin B antibiotics by an elimination mechanism not hydrolysis. Biochem 40:8877–8886

    Article  CAS  Google Scholar 

  109. Murray IA, Shaw WV (1997) O-Acetyltransferases for chloramphenicol and other natural products. Antimicrob Agent Chemother 41:1

    CAS  Google Scholar 

  110. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  CAS  PubMed  Google Scholar 

  111. Olivares J, Bedmar EJ, Sanjuán J (2013) Biological nitrogen fixation in the context of global change. Mol Plant Microb Interact 26:486–494

    Article  CAS  Google Scholar 

  112. Pankhurst CE (1977) Symbiotic effectiveness of antibiotic-resistant mutants of fast-and slow-growing strains of Rhizobium nodulating Lotus species. Can J Microbiol 23:1026–1033

    Article  CAS  PubMed  Google Scholar 

  113. Pao SS, Paulsen IT, Saier MH (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Park B, Levy S (1988) The cryptic tetracycline resistance determinant on Tn4400 mediates tetracycline degradation as well as tetracycline efflux. Antimicrob Agent Chemother 32:1797–1800

    Article  CAS  Google Scholar 

  115. Paterson DL, Bonomo RA (2005) Extended-spectrum β-lactamases: a clinical update. Clinic Microbiol Rev 18:657–686

    Article  CAS  Google Scholar 

  116. Pattison A, Skinner F (1974) The effects of antimicrobial substances on Rhizobium spp. and their use in selective media. J Appl Bacteriol 37:239–250

    Article  CAS  PubMed  Google Scholar 

  117. Paulsen IT, Skurray RA, Tam R, Saier MH, Turner RJ, Weiner JH, Goldberg EB, Grinius LL (1996) The SMR family: a novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs. Mol Microbiol 19:1167–1175

    Article  CAS  PubMed  Google Scholar 

  118. Peng G, Yuan Q, Li H, Zhang W, Tan Z (2008) Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Int J Syst Evol Microbiol 58:2158–2163

    Article  CAS  PubMed  Google Scholar 

  119. Petri W (1996) Antimicrobial agents: Sulfonamides, trimethoprim-sulfamethoxazole, quinolones, and agents for urinary tract infection. The pharmacological basis of therapeutics, 9th edn. Mac Millan, New York

    Google Scholar 

  120. Pommier Y, Leo E, Zhang H, Marchand C (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 17:421–433

    Article  CAS  PubMed  Google Scholar 

  121. Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B (2012) Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob Agent Chemother 56:1434–1443

    Article  CAS  Google Scholar 

  122. Raina J, Modi V (1972) Deoxyribonucleate binding and transformation in Rhizobium japonicum. J Bacteriol 111:356–360

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Ramirez ME, Israel DW, Wollum A (1997) Phenotypic and genotypic diversity of similar serotypes of soybean bradyrhizobia from two soil populations. Soil Biol Biochem 29:1539–1545

    Article  CAS  Google Scholar 

  124. Ramírez-Bahena M-H, Chahboune R, Peix A, Velázquez E (2013) Reclassification of Agromonas oligotrophica into the genus Bradyrhizobium as Bradyrhizobium oligotrophicum comb. nov. Int J Syst Evol Microbiol 63:1013–1016

    Article  PubMed  Google Scholar 

  125. Ramírez-Bahena MH, Peix A, Rivas R, Camacho M, Rodríguez-Navarro DN, Mateos PF, Martínez-Molina E, Willems A, Velázquez E (2009) Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int J Syst Evol Microbiol 59:1929–1934

    Article  PubMed  Google Scholar 

  126. Ramos MLG, Magalhães NF, Boddey RM (1987) Native and inoculated rhizobia isolated from field grown Phaseolus vulgaris: effects of liming an acid soil on antibiotic resistance. Soil Biol Biochem 19:179–185

    Article  CAS  Google Scholar 

  127. Ribeiro RA, Rogel MA, Lopez-Lopez A, Ormeno-Orrillo E, Barcellos FG, Martinez J, Thompson FL, Martinez-Romero E, Hungria M (2012) Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol 62:1179–1184

    Article  PubMed  Google Scholar 

  128. Rincón-Rosales R, Villalobos-Escobedo JM, Rogel MA, Martinez J, Ormeño-Orrillo E, Martínez-Romero E (2013) Rhizobium calliandrae sp. nov., Rhizobium mayense sp. nov. and Rhizobium jaguaris sp. nov., rhizobial species nodulating the medicinal legume Calliandra grandiflora. Int J Syst Evol Microbiol 63:3423–3429

    Article  PubMed  CAS  Google Scholar 

  129. Rivas R, Willems A, Palomo JL, García-Benavides P, Mateos PF, Martínez-Molina E, Gillis M, Velázquez E (2004) Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int J Syst Evol Microbiol 54:1271–1275

    Article  CAS  PubMed  Google Scholar 

  130. Roughley R, Wahab FA, Sundram J (1992) Intrinsic resistance to streptomycin and spectinomycin among root-nodule bacteria from Malaysian soils. Soil Biol Biochem 24:715–716

    Article  CAS  Google Scholar 

  131. Saïdi S, Ramírez-Bahena M-H, Santillana N, Zúñiga D, Álvarez-Martínez E, Peix A, Mhamdi R, Velázquez E (2014) Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int J Syst Evol Microbiol 64:242–247

    Article  PubMed  CAS  Google Scholar 

  132. Saier M, Tam R, Reizer A, Reizer J (1994) Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11:841–847

    Article  CAS  PubMed  Google Scholar 

  133. Salian S, Matt T, Akbergenov R, Harish S, Meyer M, Duscha S, Shcherbakov D, Bernet BB, Vasella A, Westhof E (2012) Structure-activity relationships among the kanamycin aminoglycosides: role of ring I hydroxyl and amino groups. Antimicrob Agent Chemother 56:6104–6108

    Article  CAS  Google Scholar 

  134. Sarmah AK, Meyer MT, Boxall AB (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759

    Article  CAS  PubMed  Google Scholar 

  135. Schifano JM, Edifor R, Sharp JD, Ouyang M, Konkimalla A, Husson RN, Woychik NA (2013) Mycobacterial toxin MazF-mt6 inhibits translation through cleavage of 23S rRNA at the ribosomal A site. Proc Nat Acad Sci 110:8501–8506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Schlünzen F, Zarivach R, Harms J, Bashan A, Tocilj A, Albrecht R, Yonath A, Franceschi F (2001) Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413:814–821

    Article  PubMed  Google Scholar 

  137. Scholla MH, Elkan GH (1984) Rhizobium fredii sp. nov., a fast-growing species that effectively nodulates soybeans. Int J Syst Bacteriol 34:484–486

    Article  Google Scholar 

  138. Schwarz S, Kehrenberg C, Doublet B, Cloeckaert A (2004) Molecular basis of bacterial resistance to chloramphenicol and florfenicol. FEMS Microbiol Rev 28:519–542

    Article  CAS  PubMed  Google Scholar 

  139. Sharma P, Anand R, Lakshminarayana K (1991) Construction of Tn5 tagged mutants of Rhizobium spp (Cicer) for ecological studies. Soil Biol Biochem 23:881–885

    Article  Google Scholar 

  140. Shishido M, Pepper I (1990) Identification of dominant indigenous Rhizobium meliloti by plasmid profiles and intrinsic antibiotic resistance. Soil Biol Biochem 22:11–16

    Article  Google Scholar 

  141. Sik T, Orosz L (1971) Chemistry and genetics of Rhizobium meliloti phage 16-3. Plant Soil 35:57–62

    Article  Google Scholar 

  142. Silva FV, De Meyer SE, Simões-Araújo JL, da Costa Barbé T, Xavier GR, O’Hara G, Ardley JK, Rumjanek NG, Willems A, Zilli JE (2014) Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils. Int J Syst Evol Microbiol 64:2358–2363

    Article  CAS  PubMed  Google Scholar 

  143. Simon T, Kalalova S (1996) Preparation of antibiotic resistant mutants of rhizobia and their use. Rostlinna Vyroba-UZPI (Czech Republic)

  144. Sinclair MJ, Eaglesham AR (1984) Intrinsic antibiotic resistance in relation to colony morphology in three populations of West African cowpea rhizobia. Soil Biol Biochem 16:247–251

    Article  CAS  Google Scholar 

  145. Singh SK, Jaiswal SK, Vaishampayan A, Dhar B (2013) Physiological behavior and antibiotic response of soybean (Glycine max L.) nodulating rhizobia isolated from Indian soils. Afr J Microbiol Res 7:2093–2102

    Google Scholar 

  146. Sköld O (2001) Resistance to trimethoprim and sulfonamides. Vet Res 32:261–273

    Article  PubMed  Google Scholar 

  147. Spratt BG (1994) Resistance to antibiotics mediated by target alterations. Science 264:388–393

    Article  CAS  PubMed  Google Scholar 

  148. Storm DR, Rosenthal KS, Swanson PE (1977) Polymyxin and related peptide antibiotics. Ann Rev Biochem 46:723–763

    Article  CAS  PubMed  Google Scholar 

  149. Subramaniam B, Babu C (1993) Intrinsic antibiotic resistance among rhizobia isolated from sub-tropical Himalayan legumes. Soil Biol Biochem 25:1057–1060

    Article  Google Scholar 

  150. Tenover FC (2006) Mechanisms of antimicrobial resistance in bacteria. Am J Med 119:S3–S10

    Article  CAS  PubMed  Google Scholar 

  151. Thomashow LS, Weller DM, Bonsall RF, Pierson LS (1990) Production of the antibiotic phenazine-1-carboxylic acid by fluorescent Pseudomonas species in the rhizosphere of wheat. Appl Environ Microbiol 56:908–912

    CAS  PubMed  PubMed Central  Google Scholar 

  152. Tian CF, Wang ET, Wu LJ, Han TX, Chen WF, Gu CT, Gu JG, Chen WX (2008) Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int J Syst Evol Microbiol 58:2871–2875

    Article  CAS  PubMed  Google Scholar 

  153. Turco R, Bezdicek D (1987) Diversity within two serogroups of Rhizobium leguminosarum native to soils in the Palouse of eastern Washington. Ann Appl Biol 111:103–114

    Article  Google Scholar 

  154. Turpin PE, Dhir VK, Maycroft KA, Rowlands C, Wellington EM (1992) The effect of Streptomyces species on the survival of Salmonella in soil. FEMS Microbiol Lett 101:271–280

    Google Scholar 

  155. Valverde A, Igual JM, Peix A, Cervantes E, Velazquez E (2006) Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol 56:2631–2637

    Article  CAS  PubMed  Google Scholar 

  156. van Hoek AH, Mevius D, Guerra B, Mullany P, Roberts AP, Aarts HJ (2011) Acquired antibiotic resistance genes: an overview. Front Microbiol 2:1–27

    Google Scholar 

  157. Vinuesa P, León-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Pérez-Galdona R, Werner D, Martínez-Romero E (2005) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575

    Article  CAS  PubMed  Google Scholar 

  158. Von Rechenberg M, Blake BK, Ho YSJ, Zhen Y, Chepanoske CL, Richardson BE, Xu N, Kery V (2005) Ampicillin/penicillin-binding protein interactions as a model drug-target system to optimize affinity pull-down and mass spectrometric strategies for target and pathway identification. Proteomics 5:1764–1773

    Article  CAS  Google Scholar 

  159. Wang E, Van Berkum P, Beyene D, Sui X, Dorado O, Chen W, Martínez-Romero E (1998) Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int J Syst Bacteriol 48:687–699

    Article  CAS  PubMed  Google Scholar 

  160. Wang ET, Chen WF, Sui XH, Zhang XX, Liu HC, Chen WX (2011) Rhizobium herbae sp. nov. and Rhizobium giardinii-related bacteria, minor microsymbionts of various wild legumes in China. Int J Syst Evol Microbiol 61:1912–1920

    Article  PubMed  CAS  Google Scholar 

  161. Wang R, Chang YL, Zheng WT, Zhang D, Zhang XX, Sui XH, Wang ET, Hu JQ, Zhang LY, Chen WX (2013) Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst Appl Microbiol 36:101–105

    Article  PubMed  CAS  Google Scholar 

  162. Wei GH, Tan ZY, Zhu ME, Wang ET, Han SZ, Chen WX (2003) Characterization of rhizobia isolated from legume species within the genera Astragalus and Lespedeza grown in the Loess Plateau of China and description of Rhizobium loessense sp. nov. Int J Syst Evol Microbiol 53:1575–1583

    Article  CAS  PubMed  Google Scholar 

  163. Wei GH, Wang ET, Tan ZY, Zhu ME, Chen WX (2002) Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52:2231–2239

    CAS  PubMed  Google Scholar 

  164. Wiener P (1996) Experimental studies on the ecological role of antibiotic production in bacteria. Evolut Ecol 10:405–421

    Article  Google Scholar 

  165. Wright GD (2005) Bacterial resistance to antibiotics: enzymatic degradation and modification. Adv Drug Deliver Rev 57:1451–1470

    Article  CAS  Google Scholar 

  166. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186

    Article  CAS  PubMed  Google Scholar 

  167. Xavier G, Martins L, Neves M, Rumjanek N (1998) Edaphic factors as determinants for the distribution of intrinsic antibiotic resistance in a cowpea rhizobia population. Biol Fertil Soils 27:386–392

    Article  CAS  Google Scholar 

  168. Xiong W, Sun Y, Zhang T, Ding X, Li Y, Wang M, Zeng Z (2015) Antibiotics, Antibiotic Resistance Genes, and Bacterial Community Composition in Fresh Water Aquaculture Environment in China. Microb Ecol 70:425–432

    Article  CAS  PubMed  Google Scholar 

  169. Xu L, Ge C, Cui Z, Li J, Fan H (1995) Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 45:706–711

    Article  CAS  PubMed  Google Scholar 

  170. Xu L, Shi JF, Zhao P, Chen WM, Qin W, Tang M, Wei GH (2011) Rhizobium sphaerophysae sp. nov., a novel species isolated from root nodules of Sphaerophysa salsula in China. Antonie Van Leeuwenhoek 99:845–854

    Article  PubMed  Google Scholar 

  171. Yang W, Moore IF, Koteva KP, Bareich DC, Hughes DW, Wright GD (2004) TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. J Biol Chem 279:52346–52352

    Article  CAS  PubMed  Google Scholar 

  172. Yao LJ, Shen YY, Zhan JP, Xu W, Cui GL, Wei GH (2012) Rhizobium taibaishanense sp. nov., isolated from a root nodule of Kummerowia striata. Int J Syst Evol Microbiol 62:335–341

    Article  CAS  PubMed  Google Scholar 

  173. Yu X, Cloutier S, Tambong JT, Bromfield ES (2014) Bradyrhizobium ottawaense sp. nov., a symbiotic nitrogen fixing bacterium from root nodules of soybeans in Canada. Int J Syst Evol Microbiol 64:3202–3207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    CAS  PubMed  PubMed Central  Google Scholar 

  175. Zelazna-Kowalska I (1971) Correlation between streptomycin resistance and infectiveness in Rhizobium trifolii. Plant Soil 35:67–71

    Article  Google Scholar 

  176. Zelazna-Kowalska I, Lorkiewicz Z (1971) Transformation in Rhizobium trifolii IV. Correlation between streptomycin resistance and infectiveness in Rhizobium trifolii. Acta Microbiol Pol Ser A 3:11

    CAS  Google Scholar 

  177. Zhang RJ, Hou BC, Wang ET, Li Y, Zhang XX, Chen WX (2011) Rhizobium tubonense sp. nov., isolated from root nodules of Oxytropis glabra. Int J Syst Evol Microbiol 61:512–517

    Article  CAS  PubMed  Google Scholar 

  178. Zhang YM, Li Y, Chen WF, Wang ET, Sui XH, Li QQ, Zhang YZ, Zhou YG, Chen WX (2012) Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules. Int J Syst Evol Microbiol 62:1951–1957

    Article  CAS  PubMed  Google Scholar 

  179. Zilli JE, Baraúna AC, da Silva K, De Meyer SE, Farias EN, Kaminski PE, da Costa IB, Ardley JK, Willems A, Camacho NN (2014) Bradyrhizobium neotropicale sp. nov., isolated from effective nodules of Centrolobium paraense. Int J Syst Evol Microbiol 64:3950–3957

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported with grants from the Bill and Melinda Gates Foundation Project on Capacity Building in Legume Sciences in Africa, the South African Department of Science and Technology, the Tshwane University of Technology, the National Research Foundation in Pretoria, and the South African Research Chair in Agrochemurgy and Plant Symbioses. JN is grateful for a competitive fellowship from the Bill and Melinda Gates Foundation Project on Capacity Building in Legume Sciences in Africa.

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Naamala, J., Jaiswal, S.K. & Dakora, F.D. Antibiotics Resistance in Rhizobium: Type, Process, Mechanism and Benefit for Agriculture. Curr Microbiol 72, 804–816 (2016). https://doi.org/10.1007/s00284-016-1005-0

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