Plasmid Rearrangements and Changes in Cell-Surface Architecture and Social Behavior of Azospirillum brasilense

Chapter

Abstract

Azospirilla are well-known plant-beneficial α-proteobacteria. However, they have been isolated not only from a wide range of plant, soil, and water locations, but also from human tissues. Thus, it is not surprising that these highly adaptable bacteria have flexible genomes, composed of several large replicons. In this chapter, experimental data on plasmid plasticity in the type strain A. brasilense Sp7 and in the facultative endophyte A. brasilense Sp245 are discussed. It is shown that certain changes in the primary structure of an 85-MDa plasmid of strain Sp245 were accompanied by alterations in flagellar formation and in bacterial social motility on soft media; e.g., shifts between flagellar-dependent swarming or flagellar-independent microcolonial spreading were noticed. A spontaneous reorganization of 85- and 120-MDa plasmids gave rise to an A. brasilense Sp245 derivative with a novel cell-surface architecture and with altered social motility and biofilm formation. Spontaneous changes in the plasmid profile of A. brasilense Sp7 derivatives encompassing 90- and 115-MDa replicons were concurrent with variations in the colony morphology, cell antigenic structure, swarming, and biofilm formation on abiotic surfaces and plant roots. Such genetic and physiological plasticity of azospirilla is expected to be of significance for their survival in natural environments.

Keywords

Surfactant Carbohydrate Toluene Polysaccharide Nitrite 

Notes

Acknowledgments

All my past and present collaborators are gratefully acknowledged for contributing to the work on azospirilla described in this review. I also thank Dr. Andrei V. Shelud’ko for his help with figures. Research in my lab is currently supported by grants 12-04-00262-a (to E.I. Katsy) and 13-04-01276-a (to L.P. Petrova) from the Russian Foundation for Basic Research.

References

  1. Acosta-Cruz E, Wisniewski-Dyé F, Rouy Z et al (2012) Insights into the 1.59-Mbp largest plasmid of Azospirillum brasilense CBG497. Arch Microbiol 194:725–736PubMedCrossRefGoogle Scholar
  2. Arruebarrena Di Palma A, Pereyra C, Moreno Ramirez L et al (2013) Denitrification derived nitric oxide modulates biofilm formation in Azospirillum brasilense. FEMS Microbiol Lett 338:77–85PubMedCrossRefGoogle Scholar
  3. Assmus B, Hutzler P, Kirchhof G et al (1995) In situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled, rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl Environ Microbiol 61:1013–1019PubMedCentralPubMedGoogle Scholar
  4. Baldani VLD, Baldani JI, Döbereiner J (1983) Effects of Azospirillum inoculation on root infection and nitrogen incorporation in wheat. Can J Microbiol 29:924–929CrossRefGoogle Scholar
  5. Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136CrossRefGoogle Scholar
  6. Bastarrachea F, Zamudio M, Rivas R (1988) Non-encapsulated mutants of Azospirillum brasilense and Azospirillum lipoferum. Can J Microbiol 34:24–29CrossRefGoogle Scholar
  7. Ben-Jacob E (2008) Social behavior of bacteria: from physics to complex organization. Eur Phys J B 65:315–322CrossRefGoogle Scholar
  8. Boiko AS, Smol’kina ON, Fedonenko YP et al (2010) O-Polysaccharide structure in serogroup I azospirilla. Microbiology 79:197–205CrossRefGoogle Scholar
  9. Borisov IV, Schelud’ko AV, Petrova LP, Katsy EI (2009) Changes in Azospirillum brasilense motility and the effect of wheat seedling exudates. Microbiol Res 164:578–587PubMedCrossRefGoogle Scholar
  10. Burdman S, Jurkevitch E, Okon Y (2000) Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Crit Rev Microbiol 26:91–110PubMedCrossRefGoogle Scholar
  11. Cohen MF, Han XY, Mazzola M (2004) Molecular and physiological comparison of Azospirillum spp. isolated from Rhizoctonia solani mycelia, wheat rhizosphere, and human skin wounds. Can J Microbiol 50:291–297PubMedCrossRefGoogle Scholar
  12. Croes CL, Moens S, van Bastelaere E et al (1993) The polar flagellum mediates Azospirillum brasilense adsorption to wheat roots. J Gen Microbiol 139:2261–2269CrossRefGoogle Scholar
  13. de Bruijn FJ (1992) Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergenic consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol 58:2180–2187PubMedCentralPubMedGoogle Scholar
  14. Eskew DL, Focht DD, Ting IP (1977) Nitrogen fixation, denitrification, and pleomorphic growth in a highly pigmented Spirillum lipoferum. Appl Environ Microbiol 34:582–585PubMedCentralPubMedGoogle Scholar
  15. Evseeva NV, Matora LY, Burygin GL et al (2011) Effect of Azospirillum brasilense Sp245 lipopolysaccharide on the functional activity of wheat root meristematic cells. Plant Soil 346:181–188CrossRefGoogle Scholar
  16. Fancelli S, Castaldini M, Ceccherini MT et al (1998) Use of random amplified polymorphic DNA markers for the detection of Azospirillum strains in soil microcosms. Appl Microbiol Biotechnol 49:221–225CrossRefGoogle Scholar
  17. Fedonenko YP, Zatonsky GV, Konnova SA et al (2002) Structure of the O-specific polysaccharide of the lipopolysaccharide of Azospirillum brasilense Sp245. Carbohydr Res 337:869–872PubMedCrossRefGoogle Scholar
  18. Fedonenko YP, Zdorovenko EL, Konnova SA et al (2004) Comparison of the lipopolysaccharides and O-specific polysaccharides of Azospirillum brasilense Sp245 and its Omegon-Km mutants KM018 and KM252. Microbiology 73:180–187PubMedCrossRefGoogle Scholar
  19. Fedonenko YP, Borisov IV, Konnova ON et al (2005) Determination of the structure of the repeated unit of the Azospirillum brasilense SR75 O-specific polysaccharide and homology of the lps loci in the plasmids of Azospirillum brasilense strains SR75 and Sp245. Microbiology 74:542–548CrossRefGoogle Scholar
  20. Fedonenko YP, Katsy EI, Petrova LP et al (2010) The structure of the O-specific polysaccharide from a mutant of nitrogen-fixing rhizobacterium Azospirillum brasilense Sp245 with an altered plasmid content. Russ J Bioorg Chem 36:219–223CrossRefGoogle Scholar
  21. Fellay R, Krisch HM, Prentki P, Frey J (1989) Omegon-Km: a transposable element designed for in vivo insertional mutagenesis and cloning of genes in gram-negative bacteria. Gene 76:215–226PubMedCrossRefGoogle Scholar
  22. Fibach-Paldi S, Burdman S, Okon Y (2012) Key physiological properties contributing to rhizosphere adaptation and plant growth promoting abilities of Azospirillum brasilense. FEMS Microbiol Lett 326:99–108PubMedCrossRefGoogle Scholar
  23. Fischer SE, Miguel MJ, Mori GB (2003) Effect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress. FEMS Microbiol Lett 219:53–62PubMedCrossRefGoogle Scholar
  24. Hall PG, Krieg NR (1983) Swarming of Azospirillum brasilense on solid media. Can J Microbiol 29:1592–1594CrossRefGoogle Scholar
  25. Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273PubMedCrossRefGoogle Scholar
  26. Helsel LO, Hollis DG, Steigerwalt AG, Levett PN (2006) Reclassification of Roseomonas fauriae Rihs et al. 1998 as a later heterotypic synonym of Azospirillum brasilense Tarrand et al. 1979. Int J Syst Evol Microbiol 56:2753–2755PubMedCrossRefGoogle Scholar
  27. Hogue R, Graves M, Moler S, Janda JM (2007) Pink-pigmented non-fermentative gram-negative rods associated with human infections: a clinical and diagnostic challenge. Infection 35:126–133PubMedCrossRefGoogle Scholar
  28. Jiang Z-Y, Rushing BG, Bai Y, Bauer C (1998) Isolation of Rhodospirillum centenum mutants defective in phototactic colony motility by transposon mutagenesis. J Bacteriol 180:1248–1255PubMedCentralPubMedGoogle Scholar
  29. Kaneko T, Minamisawa K, Isawa T et al (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50PubMedCentralPubMedCrossRefGoogle Scholar
  30. Katsy EI (1992) Plasmid p85 from Azospirillum brasilense Sp245: study of the possible host range and incompatibility with plasmids of Azospirillum brasilense Sp7. Mol Gen Mikrobiol Virusol 9:8–10Google Scholar
  31. Katsy EI (2011) Plasmid plasticity in the plant-associated bacteria of the genus Azospirillum. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin, pp 139–157CrossRefGoogle Scholar
  32. Katsy EI, Prilipov AG (2009) Mobile elements of an Azospirillum brasilense Sp245 85-MDa plasmid involved in replicon fusions. Plasmid 62:22–29PubMedCrossRefGoogle Scholar
  33. Katsy EI, Zhuravleva EA, Panasenko VI (1990) Transposon mutagenesis and mobilization of plasmids in the nitrogen-fixing bacterium Azospirillum brasilense Sp245. Mol Gen Mikrobiol Virusol 2:29–32PubMedGoogle Scholar
  34. Katsy EI, Borisov IV, Mashkina AB, Panasenko VI (1994) Effect of plasmid composition on the chemotaxis reaction of Azospirillum brasilense Sp245 associated with Gramineae. Mol Gen Mikrobiol Virusol 2:29–32PubMedGoogle Scholar
  35. Katsy EI, Borisov IV, Petrova LP, Matora LY (2002) The use of fragments of the 85- and 120-MDa plasmids of Azospirillum brasilense Sp245 to study the plasmid rearrangement in this bacterium and to search for homologous sequences in plasmids of Azospirillum brasilense Sp7. Russ J Genet 38:124–131CrossRefGoogle Scholar
  36. Katsy EI, Petrova LP, Kulibyakina OV, Prilipov AG (2010) Analysis of Azospirillum brasilense plasmid loci coding for (lipo)polysaccharide synthesis enzymes. Microbiology 79:216–222CrossRefGoogle Scholar
  37. Katupitiya S, Millet J, Vesk M et al (1995) A mutant of Azospirillum brasilense Sp7 impaired in flocculation with a modified colonization pattern and superior nitrogen fixation in association with wheat. Appl Environ Microbiol 61:1987–1995PubMedCentralPubMedGoogle Scholar
  38. Katzy E, Petrova L, Borisov I, Panasenko V (1995) Genetic aspects of indole acetate production in Azospirillum brasilense Sp245. In: Fendrik I, Del Gallo M, Vanderleyden J, de Zamaroczy M (eds) Azospirillum VI and related microorganisms: genetics, physiology, ecology. NATO ASI series, vol G 37. Springer, Berlin, pp 113–119Google Scholar
  39. Katzy EI, Matora LY, Serebrennikova OB, Scheludko AV (1998) Involvement of a 120-MDa plasmid of Azospirillum brasilense Sp245 in the production of lipopolysaccharides. Plasmid 40:73–83PubMedCrossRefGoogle Scholar
  40. Katzy EI, Borisov IV, Scheludko AV (2001) Effect of the integration of vector pJFF350 into plasmid 85-MDa of Azospirillum brasilense Sp245 on bacterial flagellation and motility. Russ J Genet 37:129–134CrossRefGoogle Scholar
  41. Khalsa-Moyers GK (2010) Use of proteomics tools to investigate protein expression in Azospirillum brasilense. Dissertation, University of Tennessee, KnoxvilleGoogle Scholar
  42. Kirchhof G, Schloter M, Assmus B, Hartmann A (1997) Molecular microbial ecology approaches applied to diazotrophs associated with non-legumes. Soil Biol Biochem 29:853–862CrossRefGoogle Scholar
  43. Knirel YA (2011) Structure of O-antigens. In: Knirel YA, Valvano MA (eds) Bacterial lipopolysaccharides: structure, chemical synthesis, biogenesis and interaction with host cells. Springer, Berlin, pp 41–116CrossRefGoogle Scholar
  44. Konnova ON, Boiko AS, Burygin GL et al (2008) Chemical and serological studies of lipopolysaccharides of bacteria of the genus Azospirillum. Microbiology 77:305–312CrossRefGoogle Scholar
  45. Kovtunov EA, Shelud’ko AV, Katsy EI (2012) Alterations in the primary structure of an 85-MDa plasmid affecting flagellation and motility in the bacterium Azospirillum brasilense Sp245. Russ J Genet 48:125–128CrossRefGoogle Scholar
  46. Lerner A, Castro-Sowinski S, Valverde A et al (2009a) The Azospirillum brasilense Sp7 noeJ and noeL genes are involved in extracellular polysaccharide biosynthesis. Microbiology 155:4058–4068PubMedCrossRefGoogle Scholar
  47. Lerner A, Okon Y, Burdman S (2009b) The wzm gene located on the pRhico plasmid of Azospirillum brasilense Sp7 is involved in lipopolysaccharide synthesis. Microbiology 155:791–804PubMedCrossRefGoogle Scholar
  48. Lerner A, Valverde A, Castro-Sowinski S et al (2010) Phenotypic variation in Azospirillum brasilense exposed to starvation. Environ Microbiol Rep 2:577–586PubMedCrossRefGoogle Scholar
  49. López D, Vlamakis H, Kolter R (2010) Biofilms. Cold Spring Harb Perspect Biol 2:a000398PubMedCrossRefGoogle Scholar
  50. Matora LY, Serebrennikova OB, Petrova LP et al (2003) Atypical R–S dissociation in Azospirillum brasilense. Microbiology 72:48–51CrossRefGoogle Scholar
  51. Matora LY, Burygin GL, Shchyogolev SY (2008) Study of immunochemical heterogeneity of Azospirillum brasilense lipopolysaccharides. Microbiology 77:166–170CrossRefGoogle Scholar
  52. Matveev VY, Petrova LP, Zhuravleva EA, Panasenko VI (1987) Characteristics of dissociation in cultures of Azospirillum brasilense Sp7. Mol Gen Mikrobiol Virusol 8:16–18PubMedGoogle Scholar
  53. Maughan H, Cunningham KS, Wang PW et al (2012) Pulmonary bacterial communities in surgically resected noncystic fibrosis bronchiectasis lungs are similar to those in cystic fibrosis. Pulm Med 2012:746358. doi: 10.1155/2012/746358 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Michiels K, Croes C, Vanderleyden J (1991) Two different modes of attachment of Azospirillum brasilense Sp7 to wheat roots. J Gen Microbiol 137:2241–2246CrossRefGoogle Scholar
  55. Molina-Favero C, Creus CM, Simontacchi M et al (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant Microbe Interact 21:1001–1009PubMedCrossRefGoogle Scholar
  56. Pagnier I, Raoult D, La Scola B (2008) Isolation and identification of amoeba-resisting bacteria from water in human environment by using an Acanthamoeba polyphaga co-culture procedure. Environ Microbiol 10:1135–1144PubMedCrossRefGoogle Scholar
  57. Perez-Martin J, Rojo F, de Lorenzo V (1994) Promoters responsive to DNA bending: a common theme in prokaryotic gene expression. Microbiol Rev 58:268–290PubMedCentralPubMedGoogle Scholar
  58. Petrova LP, Borisov IV, Katsy EI (2005a) Plasmid rearrangements in Azospirillum brasilense. Microbiology 74:495–497CrossRefGoogle Scholar
  59. Petrova LP, Matora LY, Burygin GL et al (2005b) Analysis of DNA, a number of cultural and morphological properties, and lipopolysaccharide structure in closely related strains of Azospirillum brasilense. Microbiology 74:188–193CrossRefGoogle Scholar
  60. Petrova LP, Shelud’ko AV, Katsy EI (2010a) Plasmid rearrangements and alterations in Azospirillum brasilense biofilm formation. Microbiology 79:120–123CrossRefGoogle Scholar
  61. Petrova LP, Varshalomidze OE, Shelud’ko AV, Katsy EI (2010b) Localization of denitrification genes in plasmid DNA of bacteria Azospirillum brasilense. Russ J Genet 46:798–804CrossRefGoogle Scholar
  62. Pothier JF, Prigent-Combaret C, Haurat J et al (2008) Duplication of plasmid-borne nitrite reductase gene nirK in the wheat-associated plant growth-promoting rhizobacterium Azospirillum brasilense Sp245. Mol Plant Microbe Interact 21:831–842PubMedCrossRefGoogle Scholar
  63. Rihs JD, Brenner DJ, Weaver RE et al (1993) Roseomonas, a new genus associated with bacteremia and other human infections. J Clin Microbiol 31:3275–3283PubMedCentralPubMedGoogle Scholar
  64. Sant’Anna F, Almeida LGP, Cecagno R et al (2011) Genomic insights into the versatility of the plant growth-promoting bacterium Azospirillum amazonense. BMC Genomics 12:409PubMedCentralPubMedCrossRefGoogle Scholar
  65. Schelud’ko AV, Makrushin KV, Tugarova AV et al (2009) Changes in motility of the rhizobacterium Azospirillum brasilense in the presence of plant lectins. Microbiol Res 164:149–156PubMedCrossRefGoogle Scholar
  66. Scheludko AV, Katsy EI, Ostudin NA et al (1998) Novel classes of Azospirillum brasilense mutants with defects in the assembly and functioning of polar and lateral flagella. Mol Gen Mikrobiol Virusol 4:33–37PubMedGoogle Scholar
  67. Serelis J, Papaparaskevas J, Stathi A et al (2013) Granulomatous infection of the hand and wrist due to Azospirillum spp. Diagn Microbiol Infect Dis 76:513–515Google Scholar
  68. Shelud’ko AV, Katsy EI (2001) Formation of polar bundles of pili and the behavior of Azospirillum brasilense cells in a semiliquid agar. Microbiology 70:570–575CrossRefGoogle Scholar
  69. Shelud’ko AV, Borisov IV, Krestinenko AV et al (2006) Effect of Congo Red on the motility of the bacterium Azospirillum brasilense. Microbiology 75:48–54CrossRefGoogle Scholar
  70. Shelud’ko AV, Kulibyakina OV, Shirokov AA et al (2008) The effect of mutations affecting synthesis of lipopolysaccharides and calcofluor-binding polysaccharides on biofilm formation by Azospirillum brasilense. Microbiology 77:313–317CrossRefGoogle Scholar
  71. Shelud’ko AV, Ponomareva EG, Varshalomidze OE et al (2009) Hemagglutinating activity and motility of the bacterium Azospirillum brasilense in the presence of various nitrogen sources. Microbiology 78:696–702CrossRefGoogle Scholar
  72. Shelud’ko AV, Shirokov AA, Sokolova MK et al (2010) Wheat root colonization by Azospirillum brasilense strains with different motility. Microbiology 79:688–695CrossRefGoogle Scholar
  73. Steenhoudt O, Keijers V, Okon Y, Vanderleyden J (2001) Identification and characterization of a periplasmic nitrate reductase in Azospirillum brasilense Sp245. Arch Microbiol 175:344–352PubMedCrossRefGoogle Scholar
  74. Tarrand JX, Krieg NE, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980PubMedCrossRefGoogle Scholar
  75. Toguchi A, Siano M, Burkart M, Harshey RM (2000) Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J Bacteriol 182:6308–6321PubMedCentralPubMedCrossRefGoogle Scholar
  76. Vanbleu E, Marchal K, Lambrecht M et al (2004) Annotation of the pRhico plasmid of Azospirillum brasilense reveals its role in determining the outer surface composition. FEMS Microbiol Lett 232:165–172PubMedCrossRefGoogle Scholar
  77. Vanbleu E, Choudhury BP, Carlson RW, Vanderleyden J (2005) The nodPQ genes in Azospirillum brasilense Sp7 are involved in sulfation of lipopolysaccharides. Environ Microbiol 7:1769–1774PubMedCrossRefGoogle Scholar
  78. Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606PubMedCrossRefGoogle Scholar
  79. Varshalomidze OE, Petrova LP, Shelud’ko AV, Katsy EI (2012) Spontaneous super-swarming derivatives of Azospirillum brasilense Sp245 have different DNA profiles and behavior in the presence of various nitrogen sources. Indian J Microbiol 52:689–694PubMedCentralPubMedCrossRefGoogle Scholar
  80. Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7:e1002430PubMedCentralPubMedCrossRefGoogle Scholar
  81. Wisniewski-Dyé F, Lozano L, Acosta-Cruz E et al (2012) Genome sequence of Azospirillum brasilense CBG497 and comparative analyses of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 3:576–602CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Institute of Biochemistry and Physiology of Plants and Microorganisms, Russian Academy of SciencesSaratovRussia

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