Transcriptional profiling of nitrogen fixation and the role of NifA in the diazotrophic endophyte Azoarcus sp. strain BH72

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Sarkar, Abhijit ^a   Reinhold Hurek, Barbara ^a  

^a UNIVERSITY OF BREMEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; NITROGEN; OLIGONUCLEOTIDE; TRANSCRIPTION FACTOR; TRANSCRIPTOME; BACTERIAL PROTEIN; PROTEIN BINDING; SIGMA FACTOR; TRANSACTIVATOR PROTEIN;

AEROBIC BACTERIUM; ARTICLE; AZOARCUS; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; CELL GROWTH; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE INSERTION; GENE MAPPING; GENE SEQUENCE; GENE TARGETING; GENETIC ASSOCIATION; MICROARRAY ANALYSIS; NIF GENE; NIFA GENE; NIFLA GENE; NITROGEN FIXATION; NONHUMAN; OPEN READING FRAME; PLANT MICROORGANISM INTERACTION; PREDICTION; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; REGULON; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; BINDING SITE; DRUG EFFECTS; ENDOPHYTE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY;

AZOARCUS; BACTERIAL PROTEINS; BINDING SITES; DOWN-REGULATION; ENDOPHYTES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MULTIGENE FAMILY; NITROGEN; NITROGEN FIXATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; REGULON; SIGMA FACTOR; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84895514911     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086527     Document Type: Article

References (61)

1. Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nature Reviews Microbiology 2: 621-631. (Pubitemid 39200045)
2. II signal transduction proteins, pivotal players in microbial nitrogen control. Microbiology and Molecular Biology Reviews 65: 80-105.
3. Merrick M, Edwards R (1995) Nitrogen control in bacteria. Microbiological Reviews 59: 604-622.
4. Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Current Opinion in Plant Biology 14: 435-443.
5. Reinhold-Hurek B, Hurek T, Gillis M, Hoste B, Vancanneyt M, et al. (1993) Azoarcus gen. nov., nitrogen-fixing proteobacteria associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth) and description of two species Azoarcus indigens sp. nov. and Azoarcus communis sp. nov. International Journal of Systematic Bacteriology 43: 574-584. (Pubitemid 23210440)
6. Egener T, Hurek T, Reinhold-Hurek B (1999) Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Molecular Plant Microbe Interactions 12: 813-819. (Pubitemid 29402958)
7. Hurek T, Reinhold B, Grimm B, Fendrik I, Niemann EG (1988) Occurrence of effective nitrogen-scavenging bacteria in the rhizosphere of Kallar grass. Plant & Soil 110: 339-348.
8. Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends in Microbiology 6: 139-144. (Pubitemid 28197802)
9. Hurek T, Handley L, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Molecular Plant Microbe Interactions 15: 233-242. (Pubitemid 34262133)
10. 2-fixing grass endophyte Azoarcus sp. strain BH72. Nature Biotechnology 24: 1385-1391.
11. Sarkar A, Köhler J, Hurek T, Reinhold-Hurek B (2012) A novel regulatory role of the Rnf-complex of Azoarcus sp. strain BH72. Molecular Microbiology 83: 408-422.
12. Riordan JT, Tietjen JA, Walsh CW, Gustafson JE, Whittam TS (2010) Inactivation of alternative sigma factor 54 (RpoN) leads to increased acid resistance, and alters locus of enterocyte effacement (LEE) expression in Escherichia coli O157 : H7. Microbiology 156: 719-730.
13. Gruber TM, Gross CA (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57: 441-466. (Pubitemid 37392951)
14. Yang H, Hu L, Hurek T, Reinhold-Hurek B (2010) Global characterization of the root transcriptome of a wild species of rice, Oryza longistaminata, by deep sequencing. BMC Genomics 11: 705-712.
15. 54-dependent promoter sequences. Nucleic Acids Research 27: 4305-4313.
16. N). Molecular Microbiology 10: 903-909.
17. Bush M, Dixon R (2012) The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription. Microbiology and Molecular Biology Reviews 76: 497-529.
18. Egener T, Sarkar A, Martin DE, Reinhold-Hurek B (2002) Identification of a NifL-like protein in a diazotroph of the beta-subgroup of the Proteobacteria, Azoarcus sp. strain BH72. Microbiology 148: 3203-3212. (Pubitemid 35243720)
19. Dixon R (1998) The oxygen-responsive NIFL-NIFA complex: a novel two-component regulatory system controlling nitrogenase synthesis in gamma-Proteobacteria. Archives of Microbiology 169: 371-380.
20. Hauberg-Lotte L, Klingenberg H, Scharf C, Böhm M, Plessl J, et al. (2012) Environmental factors affecting the expression of pilAB as well as the proteome and transcriptome of the grass endophyte Azoarcus sp. strain BH72. PLoS One 7: e30421. doi:30410.31371/journal.pone.0030421.
21. Yan Y, Ping S, Peng J, Han Y, Li L, et al. (2010) Global transcriptional analysis of nitrogen fixation and ammonium repression in root-associated Pseudomonas stutzeri A1501. BMC Genomics 11: 11.
22. Hamilton TL, Ludwig M, Dixon R, Boyd ES, Dos Santos PC, et al. (2011) Transcriptional profiling of nitrogen fixation in Azotobacter vinelandii. Journal of Bacteriology 193: 4477-4486.
23. Shidore T, Dinse T, Öhrlein J, Becker A, Reinhold-Hurek B (2012) Transcriptomic analysis of responses to exudates reveal genes required for rhizosphere competence of the endophyte Azoarcus sp. strain BH72. Environmental Microbiology 14: 2775-2787.
24. 2 fixation and nitrogenase "switch off" of Azoarcus sp. strain BH72. Journal of Bacteriology 183: 3752-3760.
25. Martinez-Noel G, Curatti L, Hernandez JA, Rubio LM (2011) NifB and NifEN protein levels are regulated by ClpX2 under nitrogen fixation conditions in Azotobacter vinelandii. Molecular Microbiology 79: 1182-1193.
26. II-like signal transmitter proteins in the diazotroph Azoarcus sp. BH72. Molecular Microbiology 38: 276-288.
27. Hwang W, Lee NY, Kim J, Lee MA, Kim KS, et al. (2011) Functional characterization of EpsC, a component of the type II secretion system, in the pathogenicity of Vibrio vulnificus. Infection and Immunity 79: 4068-4080.
28. Filloux A, Hachani B, Bleves S (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570-1583.
29. Hachani A, Lossi NS, Hamilton A, Jones C, Bleves S, et al. (2011) Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. Journal of Biological Chemistry 286: 12317-12327.
30. Bingle LEH, Bailey CM, Pallen MJ (2008) Type VI secretion: a beginner's guide. Current Opinion in Microbiology 11: 3-8.
31. 54 gene (rpoN). Journal of Bacteriology 173: 1125-1138.
32. Michiels J, Moris M, Dombrecht B, Verreth C, Vanderleyden J (1998) Differential regulation of Rhizobium etli rpoN2 gene expression during symbiosis and free-living growth. Journal of Bacteriology 180: 3620-3628. (Pubitemid 29115092)
33. Poggio S, Osorio A, Dreyfus G, Camarena L (2006) Transcriptional specificity of RpoN1 and RpoN2 involves differential recognition of the promoter sequences and specific interaction with the cognate activator proteins. Journal of Biological Chemistry 281: 27205-27215. (Pubitemid 44401750)
34. Arai H, Roh JH, Kaplan S (2008) Transcriptome dynamics during the transition from anaerobic photosynthesis to aerobic respiration in Rhodobacter sphaeroides 2.4.1. Journal of Bacteriology 190: 286-299.
35. Dörr J, Hurek T, Reinhold-Hurek B (1998) Type IV pili are involved in plant-microbe and fungus-microbe interactions. Molecular Microbiology 30: 7-17. (Pubitemid 28446616)
36. 2- fixing endophyte Azoarcus sp. strain BH72. Molecular Plant Microbe Interactions 20: 526-533.
37. Buschart A, Sachs S, Chen X, Herglotz J, Krause A, et al. (2012) Flagella mediate endophytic competence rather than act as MAMPS in rice - Azoarcus sp. strain BH72 interactions. Molecular Plant Microbe Interactions 25: 191-199.
38. Somers E, Ptacek D, Gysegom P, Srinivasan M, Vanderleyden J (2005) Azospirillum brasilense produces the auxin-like phenylacetic acid by using the key enzymes for indole-3-acetic acid biosynthesis. Applied and Environmental Microbiology 71: 1803-1810. (Pubitemid 40546096)
39. Law RJ, Hamlin JN, Sivro A, McCorrister SJ, Cardama GA, et al. (2008) A functional phenylacetic acid catabolic pathway is required for full pathogenicity of Burkholderia cenocepacia in the Caenorhabditis elegans host model. Journal of Bacteriology 190: 7209-7218.
40. Teufel R, Mascaraque V, Ismail W, Voss M, Perera J, et al. (2010) Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proceedings of the National Academy of Sciences of the United States of America 107: 14390-14395.
41. 54-dependent genes in Escherichia coli. Microbiology and Molecular Biology Reviews 65: 422-444.
42. 54 regulon (sigmulon) of Pseudomonas putida. Environmental Microbiology 5: 1281-1293.
43. Dombrecht B, Marchal K, Vanderleyden J, Michiels J (2002) Prediction and overview of the RpoN-regulon in closely related species of the Rhizobiales. Genome Biology 3: RESEARCH0076.0071-0076.0011.
44. O'Leary ND, O'Mahony MM, Dobson AD (2011) Regulation of phenylacetic acid uptake is sigma54 dependent in Pseudomonas putida CA-3. BMC microbiology 11: 229.
45. Krause A, Leyser B, Miché L, Battistoni F, Reinhold-Hurek B (2011) Exploring the function of alcohol dehydrogeanses during the endophytic life of Azoarcus sp. strain BH72. Molecular Plant Microbe Interactions 24: 1325-1332.
46. 54 regulon, and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation. Mol Genet Genomics 278: 255-271.
47. Tian Z, Zou H, Li J, Zhang Y, Liu Y, et al. (2006) Transcriptome analysis of Sinorhizobium meliloti nodule bacteria in nifA mutant background. Chinese Science Bulletin 51: 2079-2086. (Pubitemid 44394620)
48. Salazar E, Diaz-Mejia JJ, Moreno-Hagelsieb G, Martinez-Batallar G, Mora Y, et al. (2010) Characterization of the NifA-RpoN regulon in Rhizobium etli in free life and in symbiosis with Phaseolus vulgaris. Applied and Environmental Microbiology 76: 4510-4520.
49. Brito B, Martinez M, Fernandez D, Rey L, Cabrera E, et al. (1997) Hydrogenase genes from Rhizobium leguminosarum bv. viciae are controlled by the nitrogen fixation regulatory protein nifA. Proceedings of the National Academy of Sciences of the United States of America 94: 6019-6024. (Pubitemid 27270628)
50. Sarma AD, Emerich DW (2006) A comparative proteomic evaluation of culture grown vs nodule isolated Bradyrhizobium japonicum. Proteomics 6: 3008-3028. (Pubitemid 43806400)
51. Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon R (2004) The NifL-NifA System: a multidomain transcriptional regulatory complex that integrates environmental signals. Journal of Bacteriology 186: 601-610. (Pubitemid 38129636)
52. Dombrecht B, Heusdens C, Beullens S, Verreth C, Mulkers E, et al. (2005) Defence of Rhizobium etli bacteroids against oxidative stress involves a complexly regulated atypical 2-Cys peroxiredoxin. Molecular Microbiology 55: 1207-1221. (Pubitemid 40299188)
53. Bueno E, Mesa S, Sanchez C, Bedmar EJ, Delgado MJ (2010) NifA is required for maximal expression of denitrification genes in Bradyrhizobium japonicum. Environmental Microbiology Reports 12: 393-400.
54. Fischer H-M (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiological Reviews 58: 352-386.
55. Sanjuan J, Olivares F (1991) Multicopy Plasmids Carrying the Klebsiella pneumoniae nifA Gene Enhance Rhizobium meliloti Nodulation Competitiveness on Alfalfa. Molecular Plant Microbe Interactions 4: 365-369.
56. Ow DW, Sundaresan V, Rothstein DM, Brown SE, Ausubel FM (1983) Promoters regulated by the glnG (ntrC) and nifA gene products share a heptameric consensus sequence in the -15 region. Proceedings of the National Academy of Sciences of the United States of America 80: 2524-2528. (Pubitemid 13093349)
57. Reinhold B, Hurek T, Fendrik I (1985) Strain-specific chemotaxis of Azospirillum spp. Journal of Bacteriology 162: 190-195.
58. Bartram AK, Lynch MD, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Applied and environmental microbiology 77: 3846-3852.
59. de Jong A, Pietersma H, Cordes M, Kuipers OP, Kok J (2012) PePPER: a webserver for prediction of prokaryote promoter elements and regulons. BMC genomics 13: 299.
60. Münch R, Hiller K, Barg H, Heldt D, Linz S, et al. (2003) PRODORIC: prokaryotic database of gene regulation. Nucleic Acids Research 31: 266-269. (Pubitemid 36150381)
61. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, et al. (2003) GenDB-an open source genome annotation system for prokaryote genomes. Nucleic Acids Research 31: 2187-2195. (Pubitemid 37442085)