Comparative Genomic Analysis of N2-Fixing and Non-N2-Fixing Paenibacillus spp.: Organization, Evolution and Expression of the Nitrogen Fixation Genes

PLoS Genetics

Volumn 10, Issue 3, 2014, Pages

  Xie, Jian Bo ^a   Du, Zhenglin ^b   Bai, Lanqing ^a   Tian, Changfu ^a   Zhang, Yunzhi ^a   Xie, Jiu Yan ^a   Wang, Tianshu ^a   Liu, Xiaomeng ^a   Chen, Xi ^a   Cheng, Qi ^c   Chen, Sanfeng ^a   Li, Jilun ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGENASE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BINDING SITE; COMPARATIVE GENOMIC ANALYSIS; CONTROLLED STUDY; ESCHERICHIA COLI; ESCHERICHIA COLI JM109; FRANKIA; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENETIC HETEROGENEITY; GENETIC ORGANIZATION; GENOMICS; HESA GENE; HORIZONTAL GENE TRANSFER; MOLECULAR PHYLOGENY; NIFB GENE; NIFD GENE; NIFE GENE; NIFH GENE; NIFK GENE; NIFN GENE; NIFV GENE; NIFX GENE; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAENIBACILLUS; PROMOTER REGION; COMPARATIVE STUDY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGY;

BINDING SITES; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOMICS; MULTIGENE FAMILY; NITROGEN FIXATION; NITROGENASE; PAENIBACILLUS; PHYLOGENY; PROMOTER REGIONS, GENETIC;

EID: 84897381205     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004231     Document Type: Article

References (85)

1. Falkowski PG, (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387: 272-275.
2. Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R, (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13: 162.
3. Arnold W, Rump A, Klipp W, Priefer UB, Pühler A, (1988) Nucleotide sequence of a 24,206-base-pair DNA fragment carrying the entire nitrogen fixation gene cluster of Klebsiella pneumoniae. J Mol Biol 203: 715-738.
4. Setubal JC, dos Santos P, Goldman BS, Ertesvåg H, Espin G, et al. (2009) Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse anaerobic metabolic processes. J Bacteriol 191: 4534-4545.
5. Normand P, Bouquet J, (1989) Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol 29: 436-447.
6. Normand P, Gouy M, Cournoyer B, Simonet P, (1992) Nucleotide sequence of nifD from Frankia alni strain ArI3: phylogenetic inferences. Mol Biol Evol 9: 495-506.
7. Hartmann LS, Barnum SR, (2010) Inferring the evolutionary history of Mo-dependent nitrogen fixation from phylogenetic studies of nifK and nifDK. J Mol Evol 71: 70-85.
8. Raymond J, Siefert JL, Staples CR, Blankenship RE, (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554.
9. Leigh JA, (2000) Nitrogen fixation in methanogens: the archaeal perspective. Crit Rev Microbiol 2: 125-131.
10. Boyd E, Hamilton T, Peters J, (2011) An alternative path for the evolution of biological nitrogen fixation. Front Microbiol 2: 205 doi: 10.3389/fmicb.2011.00205.
11. Boyd E, Anbar A, Miller S, Hamilton T, Lavin M, et al. (2011) A late methanogen origin for molybdenum-dependent nitrogenase. Geobiology 9: 221-232.
12. Yan Y, Yang J, Dou Y, Chen M, Ping S, et al. (2008) Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci U S A 105: 7564-7569.
13. Pedrosa FO, Monteiro RA, Wassem R, Cruz LM, Ayub RA, et al. (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 7: e1002064.
14. Baar C, Eppinger M, Raddatz G, Simon J, Lanz C, et al. (2003) Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci U S A 100: 11690-11695.
15. Hu Y, Fay AW, Lee CC, Yoshizawa J, Ribbe MW, (2008) Assembly of nitrogenase MoFe protein. Biochemistry 47: 3973-3981.
16. Rubio LM, Ludden PW, (2008) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu Rev Microbiol 62: 93-111.
17. Kaiser JT, Hu Y, Wiig JA, Rees DC, Ribbe MW, (2011) Structure of precursor-bound NifEN: a nitrogenase FeMo cofactor maturase/insertase. Science 331: 91-94.
18. Joerger RD, Bishop PE, Evans HJ, (1988) Bacterial alternative nitrogen fixation systems. Crit Rev Microbiol 16: 1-14.
19. Rubio LM, Ludden PW, (2005) Maturation of nitrogenase: a biochemical puzzle. J Bacteriol 187: 405-414.
20. Chisnell J, Premakumar R, Bishop P, (1988) Purification of a second alternative nitrogenase from a nifHDK deletion strain of Azotobacter vinelandii. J Bacteriol 170: 27-33.
21. Davis R, Lehman L, Petrovich R, Shah VK, Roberts GP, et al. (1996) Purification and characterization of the alternative nitrogenase from the photosynthetic bacterium Rhodospirillum rubrum. J Bacteriol 178: 1445-1450.
22. Schneider K, Muller A, Schramm U, Klipp W, (1991) Demonstration of a molybdenum- and vanadium-dependent nitrogenase in a nifHDK-deletion mutant of Rhodobacter capsulatus. Eur J Biochem 195: 653-661.
23. Lal S, Tabacchioni S, (2009) Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian J Microbiol 49: 2-10.
24. McSpadden Gardener BB, (2004) Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94: 1252-1258.
25. Montes MJ, Mercadé E, Bozal N, Guinea J, (2004) Paenibacillus antarcticus sp. nov., a novel psychrotolerant organism from the Antarctic environment. Int J Syst Evol Microbiol 54: 1521-1526.
26. Ouyang J, Pei Z, Lutwick L, Dalal S, Yang L, et al. (2008) Paenibacillus thiaminolyticus: a new cause of human infection, inducing bacteremia in a patient on hemodialysis. Ann Clin Lab Sci 38: 393-400.
27. Ash C, Priest FG, Collins MD, (1993) Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Antonie van Leeuwenhoek 64: 253-260.
28. Ma Y, Xia Z, Liu X, Chen S, (2007) Paenibacillus sabinae sp. nov., a nitrogen-fixing species isolated from the rhizosphere soils of shrubs. Int J Syst Evol Microbiol 57: 6-11.
29. Ma Y, Zhang J, Chen S, (2007) Paenibacillus zanthoxyli sp. nov., a novel nitrogen-fixing species isolated from the rhizosphere of Zanthoxylum simulans. Int J Syst Evol Microbiol 57: 873-877.
30. Ma Y, Chen S, (2008) Paenibacillus forsythiae sp. nov., a nitrogen-fixing species isolated from rhizosphere soil of Forsythia mira. Int J Syst Evol Microbiol 58: 319-323.
31. Hong Y, Ma Y, Zhou Y, Gao F, Liu H, et al. (2009) Paenibacillus sonchi sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Sonchus oleraceus. Int J Syst Evol Microbiol 59: 2656-2661.
32. Jin H, Lv J, Chen S, (2011) Paenibacillus sophorae sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Sophora japonica. Int J Syst Evol Microbiol 61: 767-771.
33. Jin H, Zhou Y, Liu H, Chen S, (2011) Paenibacillus jilunlii sp. nov., a nitrogen-fixing species isolated from the rhizosphere of Begonia semperflorens. Int J Syst Evol Microbiol 61: 1350-1355.
34. Xie J, Zhang L, Zhou Y, Liu H, Chen S, (2012) Paenibacillus taohuashanense sp. nov., a nitrogen-fixing species isolated from rhizosphere soil of the root of Caragana kansuensis Pojark. Antonie van Leeuwenhoek 102: 735-741.
35. Wang L, Li J, Li QX, Chen S, (2013) Paenibacillus beijingensis sp. nov., a nitrogen-fixing species isolated from wheat rhizosphere soil. Antonie van Leeuwenhoek 104: 675-683.
36. Chow V, Nong G, John FJS, Rice JD, Dickstein E, et al. (2012) Complete genome sequence of Paenibacillus sp. strain JDR-2. Stand Genomic Sci 6: 1-10.
37. Mead DA, Lucas S, Copeland A, Lapidus A, Cheng J, et al. (2012) Complete genome sequence of Paenibacillus strain Y412MC10, a novel Paenibacillus lautus strain isolated from Obsidian hot spring in Yellowstone national park. Stand Genomic Sci 6: 381-400.
38. Ma M, Wang Z, Li L, Jiang X, Guan D, et al. (2012) Complete genome sequence of Paenibacillus mucilaginosus 3016, a bacterium functional as microbial fertilizer. J Bacteriol 194: 2777-2778.
39. Kim JF, Jeong H, Park S, Kim S, Park YK, et al. (2010) Genome sequence of the polymyxin-producing plant-probiotic rhizobacterium Paenibacillus polymyxa E681. J Bacteriol 192: 6103-6104.
40. Ma M, Wang C, Ding Y, Li L, Shen D, et al. (2011) Complete genome sequence of Paenibacillus polymyxa SC2, a strain of plant growth-promoting rhizobacterium with broad-spectrum antimicrobial activity. J Bacteriol 193: 311-312.
41. Sirota-Madi A, Olender T, Helman Y, Brainis I, Finkelshtein A, et al. (2012) Genome sequence of the pattern-forming social bacterium Paenibacillus dendritiformis C454 chiral morphotype. J Bacteriol 194: 2127-2128.
42. Ding R, Li Y, Qian C, Wu X, (2011) Draft Genome sequence of Paenibacillus elgii B69, a strain with broad antimicrobial activity. J Bacteriol 193: 4537-4537.
43. Jeong H, Choi S, Park S, Kim S, Park S, (2012) Draft genome sequence of Paenibacillus peoriae strain KCTC 3763T. J Bacteriol 194: 1237-1238.
44. Sirota-Madi A, Olender T, Helman Y, Ingham C, Brainis I, et al. (2010) Genome sequence of the pattern forming Paenibacillus vortex bacterium reveals potential for thriving in complex environments. BMC Genomics 11: 710.
45. Li N, Xia T, Xu Y, Qiu R, Xiang H, et al. (2012) Genome sequence of Paenibacillus sp. strain Aloe-11, an endophytic bacterium with broad antimicrobial activity and intestinal colonization ability. J Bacteriol 194: 2117-2118.
46. Shin SH, Kim S, Kim JY, Song HY, Cho SJ, et al. (2012) Genome sequence of Paenibacillus terrae HPL-003, a xylanase-producing bacterium isolated from soil found in forest residue. J Bacteriol 194: 1266-1266.
47. Merritt PM, Danhorn T, Fuqua C, (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189: 8005-8014.
48. Oh CJ, Kim HB, Kim J, Kim WJ, Lee H, et al. (2012) Organization of nif gene cluster in Frankia sp. EuIK1 strain, a symbiont of Elaeagnus umbellata. Arch Microbiol 194: 29-34.
49. Welsh EA, Liberton M, Stöckel J, Loh T, Elvitigala T, et al. (2008) The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle. Proc Natl Acad Sci U S A 105: 15094-15099.
50. Wang L, Zhang L, Liu Z, Zhao D, Liu X, et al. (2013) A minimal nitrogen fixation gene cluster from Paenibacillus sp. WLY78 enables expression of active nitrogenase in Escherichia coli. PLoS Genet 9: e1003865.
51. Leigh J (2005) Genomics of diazotrophic archaea. Genomes and genomics of nitrogen-fixing organisms: Springer. pp. 7-12.
52. Richter M, Rosselló-Móra R, (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106: 19126-19131.
53. Xie JB, Bai LQ, Wang LY, Chen SF, (2012) Phylogeny of 16S rRNA and nifH genes and regulation of nitrogenase activity by oxygen and ammonium in the genus Paenibacillus. Mikrobiologiia 81: 760-767.
54. Montoya JP, Voss M, Kahler P, Capone DG, (1996) A simple, high-precision, high-sensitivity tracer assay for N (inf2) fixation. Appl Environ Microbiol 62: 986-993.
55. Dixon R, Kahn D, (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2: 621-631.
56. Kormelink TG, Koenders E, Hagemeijer Y, Overmars L, Siezen RJ, et al. (2012) Comparative genome analysis of central nitrogen metabolism and its control by GlnR in the class Bacilli. BMC Genomics 13: 191-206.
57. Doroshchuk N, Gelfand M, Rodionov D, (2006) Regulation of nitrogen metabolism in gram-positive bacteria. Mol Biol 40: 829-836.
58. Zhao D, Curatti L, Rubio LM, (2007) Evidence for nifU and nifS participation in the biosynthesis of the iron-molybdenum cofactor of nitrogenase. J Biol Chem 282: 37016-37025.
59. Johnson DC, Dean DR, Smith AD, Johnson MK, (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74: 247-281.
60. Hong Y, Ma Y, Wu L, Maki M, Qin W, et al. (2012) Characterization and analysis of nifH genes from Paenibacillus sabinae T27. Microbiol Res 167: 596-601.
61. Hacker J, Carniel E, (2001) Ecological fitness, genomic islands and bacterial pathogenicity. EMBO Rep 2: 376-381.
62. Hacker J, Kaper JB, (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679.
63. Young JPW, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, et al. (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7: R34.
64. Chen JS (2005) Genomic aspects of nitrogen fixation in the Clostridia. Genomes and genomics of nitrogen-fixing organisms: Springer. pp. 13-26.
65. Dodsworth JA, Leigh JA, (2006) Regulation of nitrogenase by 2-oxoglutarate-reversible, direct binding of a PII-like nitrogen sensor protein to dinitrogenase. Proc Natl Acad Sci U S A 103: 9779-9784.
66. Dobrindt U, Hochhut B, Hentschel U, Hacker J, (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2: 414-424.
67. Hirsch AM, McKhann HI, Reddy A, Liao J, Fang Y, et al. (1995) Assessing horizontal transfer of nifHDK genes in eubacteria: nucleotide sequence of nifK from Frankia strain HFPCcI3. Mol Biol Evol 12: 16-27.
68. Nakamura Y, Itoh T, Matsuda H, Gojobori T, (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 36: 760-766.
69. Finan TM, (2002) Evolving insights: symbiosis islands and horizontal gene transfer. J Bacteriol 184: 2855-2856.
70. Sullivan JT, Ronson CW, (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci U S A 95: 5145-5149.
71. Young J (2005) The phylogeny and evolution of nitrogenases. Genomes and genomics of nitrogen-fixing organisms: Springer. pp. 221-241.
72. Galibert F, Finan TM, Long SR, Pühler A, Abola P, et al. (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293: 668-672.
73. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, et al. (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA research 7: 331-338.
74. Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, et al. (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA research 9: 189-197.
75. Li R, Li Y, Kristiansen K, Wang J, (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713-714.
76. Delcher AL, Bratke KA, Powers EC, Salzberg SL, (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
77. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS, (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39: W347-W352.
78. Zhao Y, Wu J, Yang J, Sun S, Xiao J, et al. (2012) PGAP: pan-genomes analysis pipeline. Bioinformatics 28: 416-418.
79. Darling AC, Mau B, Blattner FR, Perna NT, (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
80. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
81. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542.
82. Thompson JD, Gibson T, Higgins DG, (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2Unit 2.3. doi: 10.1002/0471250953.bi0203s00.
83. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
84. Guindon S, Dufayard J, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
85. Shimodaira H, Hasegawa M, (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246-1247.