Bacteriophage prevalence in the genus Azospirillum and analysis of the first genome sequence of an Azospirillum brasilense integrative phage

Applied and Environmental Microbiology

Volumn 74, Issue 3, 2008, Pages 861-874

  Boyer, Mickaël ^a,b,c,d   Haurat, Jacqueline ^a,b,c,d   Samain, Sylvie ^e   Segurens, Béatrice ^e   Gavory, Frédérick ^e   González, Víctor ^f   Mavingui, Patrick ^a,b,c,d   Rohr, René ^a,b,c,d   Bally, René ^a,b,c,d   Wisniewski Dyé, Florence ^a,b,c,d  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c University of Lyon   (France)

^d IFR 41   (France)

^e CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^f INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MICROBIOLOGY; PROTEINS; TRANSMISSION ELECTRON MICROSCOPY;

GEL ELECTROPHORESIS; HOMOLOGY; PHAGE MORPHOGENESIS; RHIZOBACTERIA;

BACTERIOPHAGES;

DNA; DOUBLE STRANDED DNA; MITOMYCIN C; PROTEIN;

BACTERIOPHAGE; DNA; ELECTROKINESIS; GENETIC ANALYSIS; GENOME; HYBRIDIZATION; LYSIS; PROTEIN; RHIZOBACTERIUM; TRANSMISSION ELECTRON MICROSCOPY;

ARTICLE; AZOSPIRILLUM; AZOSPIRILLUM BRASILENSE; AZOSPIRILLUM DOEBEREINERAE; AZOSPIRILLUM LIPOFERUM; BACTERIAL STRAIN; BACTERIOLYSIS; BACTERIOPHAGE; DNA HYBRIDIZATION; DNA HYBRIDIZING SIGNAL; GENE SEQUENCE; GENOME SIZE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAMETER; PARTICLE SIZE; PLASMID; PROPHAGE; PROTEIN FUNCTION; PROTEIN STRUCTURE; PULSED FIELD GEL ELECTROPHORESIS; REPLICON; SEQUENCE HOMOLOGY; UNINDEXED SEQUENCE;

AZOSPIRILLUM; AZOSPIRILLUM BRASILENSE; AZOSPIRILLUM DOEBEREINERAE; AZOSPIRILLUM LIPOFERUM; BACTERIA (MICROORGANISMS); RHIZOBIALES; SIPHOVIRIDAE;

EID: 38949145099     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02099-07     Document Type: Article

References (67)

1. Alexandre, G., and R. Bally. 1999. Emergence of a laccase-positive variant of Azospirillum lipoferum occurs via a two-step phenotypic switching process. FEMS Microbiol. Lett. 174:371-378.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Ashelford, K. E., S. J. Norris, J. C. Fry, M. J. Bailey, and M. J. Day. 2000. Seasonal population dynamics and interactions of competing bacteriophages and their host in the rhizosphere. Appl. Environ. Microbiol. 66:4193-4199.
4. Baldani, V. L. D., M. A. B. Alvarez, J. I. Baldani, and J. Doëbereiner. 1986. Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant Soil 90:37-40.
5. 2-fixing bacteria from the rhizosphere of rice. Can. J. Microbiol. 29:881-887.
6. Bartolomé, B., Y. Jubete, E. Martínez, and F. de la Cruz. 1991. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene 102:75-78.
7. Bashan, Y., G. Holguin, and L. E. de-Bashan. 2004. Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can. J. Microbiol. 50:521-577.
8. Beilstein, F., and B. Dreiseikelmann. 2006. Bacteriophages of freshwater Brevundimonas vesicularis isolates. Res. Microbiol. 157:213-219.
9. Beringer, J. F. 1974. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:188-198.
10. Broudy, T. B., V. Pancholi, and V. A. Fischetti. 2001. Induction of lysogenic bacteriophage and phage-associated toxin from group a streptococci during coculture with human pharyngeal cells. Infect. Immun. 69:1440-1443.
11. Brown, D. G., and C. Allen. 2004. Ralstonia solanacearum genes induced during growth in tomato: an inside view of bacterial wilt. Mol. Microbiol. 53:1641-1660.
12. Brüssow, H., and F. Desiere. 2001. Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol. Microbiol. 39:213-223.
13. Brüssow, H., and R. W. Hendrix. 2002. Phage genomics: small is beautiful. Cell 108:13-16.
14. Caballero-Mellado, J., L. López-Reyes, and R. Bustillos-Cristales. 1999. Presence of 16S rRNA genes in multiple replicons in Azospirillum brasilense. FEMS Microbiol. Lett. 178:283-288.
15. Canchaya, C., G. Fournous, and H. Brüssow. 2004. The impact of prophages on bacterial chromosomes. Mol. Microbiol. 53:9-18.
16. Canchaya, C., C. Proux, G. Fournous, A. Bruttin, and H. Brüssow. 2003. Prophage genomics. Microbiol. Mol. Biol. Rev. 67:238-276.
17. Casjens, S. R. 2005. Comparative genomics and evolution of the tailed-bacteriophages. Curr. Opin. Microbiol. 8:451-458.
18. Chibani-Chennoufi, S., A. Bruttin, M.-L. Dillmann, and H. Brüssow. 2004. Phage-host interaction: an ecological perspective. J. Bacteriol. 186:3677-3686.
19. Delcher, A. L., D. Harmon, S. Kasif, O. White, and S. L. Salzberg. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27:4636-4641.
20. Dobbelaere, S., A. Croonenborghs, T. Amber, D. Ptacek, J. Vanderleyden, P., C. L.-G. Dutto, J. Caballero-Mellado, J. F. Aguirre, Y. Kapulnik, S. Brener, S. Burdman, D. Kadouri, S. Sarig, and Y. Okon. 2001. Responses of agronomically important crops to inoculation with Azospirillum. Aust. J. Plant Physiol. 28:1-9.
21. Dozois, C. M., F. Daigle, and R. Curtiss III. 2003. Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. USA 100:247-252.
22. Eckert, B., O. B. Weber, G. Kirchhof, A. Halbritter, M. Stoffels, and A. Hartmann. 2001. Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus. Int. J. Syst. Evol. Microbiol. 51:17-26.
23. Elbeltagy, A., K. Nishioka, T. Sato, H. Suzuki, B. Ye, T. Hamada, T. Isawa, H. Mitsui, and K. Minamisawa. 2001. Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl. Environ. Microbiol. 67:5285-5293.
24. Elmerich, C., B. Quiviger, C. Rosenberg, C. Franche, P. Laurent, and J. Döbereiner. 1982. Characterization of a temperate bacteriophage for Azospirillum. Virology 122:29-37.
25. Eskew, D. L., D. D. Focht, and I. P. Ting. 1977. Nitrogen fixation, denitrification, and pleomorphic growth in a highly pigmented Spirillum lipoferum. Appl. Environ. Microbiol. 34:582-585.
26. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8:186-194.
27. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185.
28. Franche, C., and C. Elmerich. 1981. Physiological properties and plasmid content of several strains of Azospirillum brasilense and A. lipoferum. Ann. Microbiol. (Paris) 132:3-18.
29. Germida, J. J. 1986. Population dynamics of Azospirillum brasilense and its bacteriophage in soil. Plant Soil 90:117-128.
30. Germida, J. J. 1984. Spontaneous induction of bacteriophage during growth of Azospirillum brasilense in complex media. Can. J. Microbiol. 30:805-808.
31. Gordon, D., C. Abajian, and P. Green. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:195-202.
32. Hendrix, R. W. 2003. Bacteriophage genomics. Curr. Opin. Microbiol. 6:506-511.
33. Hynes, M. F., and N. F. McGregor. 1990. Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol. Microbiol. 4:567-574.
34. Jacoud, C., D. Job, P. Wadoux, and R. Bally. 1999. Initiation of root growth stimulation by Azospirillum lipoferum CRT1 during maize seed germination. Can. J. Microbiol. 45:339-342.
35. Kabir, M., D. Faure, T. Heulin, W. Achouak, and R. Bally. 1995. Azospirillum populations in soils infested by a parasitic weed (Striga) under Sorghum cultivation in Mali, West Africa. Eur. J. Soil Biol. 32:157-163.
36. Khammas, K. M., E. Ageron, P. A. Grimont, and P. Kaiser. 1989. Azospirillum irakense sp. nov., a nitrogen-fixing bacterium associated with rice roots and rhizosphere soil. Res. Microbiol. 140:679-693.
37. Kuroda, M., T. Ohta, I. Uchiyama, T. Baba, H. Yuzawa, I. Kobayashi, L. Cui, A. Oguchi, K. Aoki, Y. Nagai, J. Lian, T. Ito, M. Kanamori, H. Matsumaru, A. Maruyama, H. Murakami, A. Hosoyama, Y. Mizutani-Ui, N. K. Takahashi, T. Sawano, R. Inoue, C. Kaito, K. Sekimizu, H. Hirakawa, S. Kuhara, S. Goto, J. Yabuzaki, M. Kanehisa, A. Yamashita, K. Oshima, K. Furuya, C. Yoshino, T. Shiba, M. Hattori, N. Ogasawara, H. Hayashi, and K. Hiramatsu. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
38. Kwan, T., J. Liu, M. DuBow, P. Gros, and J. Pelletier. 2006. Comparative genomic analysis of 18 Pseudomonas aeruginosa bacteriophages. J. Bacteriol. 188:1184-1187.
39. Kwan, T., J. Liu, M. DuBow, P. Gros, and J. Pelletier. 2005. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc. Natl. Acad. Sci. USA 102:5174-5179.
40. Lang, A. S., and J. T. Beatty. 2007. Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol. 15:54-62.
41. Lawrence, J. G., G. F. Hatfull, and R. W. Hendrix. 2002. Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J. Bacteriol. 184:4891-4905.
42. Lohr, J. E., F. Chen, and R. T. Hill. 2005. Genomic analysis of bacteriophage ΦJL001: insights into its interaction with a sponge-associated alpha-proteobacterium. Appl. Environ. Microbiol. 71:1598-1609.
43. Marchler-Bauer, A., J. B. Anderson, P. F. Cherukuri, C. DeWeese-Scott, L. Y. Geer, M. Gwadz, S. He, D. I. Hurwitz, J. D. Jackson, Z. Ke, C. J. Lanczycki, C. A. Liebert, C. Liu, F. Lu, G. H. Marchler, M. Mullokandov, B. A. Shoemaker, V. Simonyan, J. S. Song, P. A. Thiessen, R. A. Yamashita, J. J. Yin, D. Zhang, and S. H. Bryant. 2005. CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33:D192-D196.
44. Martin-Didonet, C. C., L. S. Chubatsu, E. M. Souza, M. Kleina, F. G. Rego, L. U. Rigo, M. G. Yates, and F. O. Pedrosa. 2000. Genome structure of the genus Azospirillum. J. Bacteriol. 182:4113-4116.
45. Michiels, K., P. De Troch, I. Onyeocha, A. Van Gool, C. Elmerich, and J. Vanderleyden. 1989. Plasmid localization and mapping of two Azospirillum brasilense loci that affect exopolysaccharide synthesis. Plasmid 21:142-146.
46. Nelson, L. M., and R. Knowles. 1978. Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilense grown in continuous culture. Can. J. Microbiol. 24:1395-1403.
47. Ohnishi, M., K. Kurokawa, and T. Hayashi. 2001. Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol. 9:481-485.
48. Pedulla, M. L., M. E. Ford, J. M. Houtz, T. Karthikeyan, C. Wadsworth, J. A. Lewis, D. Jacobs-Sera, J. Falho, J. Gross, N. R. Pannunzio, W. Brucker, V. Kumar, J. Kandasamy, L. Keenan, S. Bardarov, J. Kriakov, J. G. Lawrence, W. R. Jacobs, Jr., R. W. Hendrix, and G. F. Hatfull. 2003. Origins of highly mosaic mycobacteriophage genomes. Cell 113:171-182.
49. Pothier, J. F., F. Wisniewski-Dyé, M. Weiss-Gayet, Y. Moënne-Loccoz, and C. Prigent-Combaret. 2007. Promoter trap identification of wheat seed extract-induced genes in the plant growth-promoting rhizobacterium Azospirillum brasilense Sp245. Microbiology 153:3608-3622.
50. Rohwer, F., A. Segall, G. Steward, V. Seguritan, M. Breitbart, F. Wolven, and F. Azam. 2000. The complete genomic sequence of the marine phage roseophage SIO1 shares homology with non-marine phages. Limnol. Oceanogr. 45:408-418.
51. Romero, D., S. Brom, J. Martinez-Salazar, M. L. Girard, R. Palacios, and G. Dávila. 1991. Amplification and deletion of a nod-nif region in the symbiotic plasmid of Rhizobium phaseoli. J. Bacteriol. 173:2435-2441.
52. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajandream, and B. Barrell. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
54. Schnabel, E. L., and A. L. Jones. 2001. Isolation and characterization of five Erwinia amylovora bacteriophages and assessment of phage resistance in strains of Erwinia amylovora. Appl. Environ. Microbiol. 67:59-64.
55. Silander, O. K., D. M. Weinreich, K. M. Wright, K. J. O'Keefe, C. U. Rang, P. E. Turner, and L. Chao. 2005. Widespread genetic exchange among terrestrial bacteriophages. Proc. Natl. Acad. Sci. USA 102:19009-19014.
56. Stanton, T. B. 2007. Prophage-like gene transfer agents - novel mechanisms of gene exchange for Methanococcus, Desulfovibrio, Brachyspira, and Rhodobacter species. Anaerobe 13:43-49.
57. Suttle, C. A. 2005. Viruses in the sea. Nature 437:356-361.
58. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
59. Tarrand, J. J., N. R. Krieg, and J. Döbereiner. 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. 24:967-980.
60. Tettelin, H., V. Masignani, M. J. Cieslewicz, C. Donati, D. Medini, N. L. Ward, S. V. Angiuoli, J. Crabtree, A. L. Jones, A. S. Durkin, R. T. Deboy, T. M. Davidsen, M. Mora, M. Scarselli, I. Margarit y Ros, J. D. Peterson, C. R. Hauser, J. P. Sundaram, W. C. Nelson, R. Madupu, L. M. Brinkac, R. J. Dodson, M. J. Rosovitz, S. A. Sullivan, S. C. Daugherty, D. H. Haft, J. Selengut, M. L. Gwinn, L. Zhou, N. Zafar, H. Khouri, D. Radune, G. Dimitrov, K. Watkins, K. J. O'Connor, S. Smith, T. R. Utterback, O. White, C. E. Rubens, G. Grandi, L. C. Madoff, D. L. Kasper, J. L. Telford, M. R. Wessels, R. Rappuoli, and C. M. Fraser. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome." Proc. Natl. Acad. Sci. USA 102:13950-13955.
61. Trân Vân, V., O. Berge, D. Faure, R. Bally, P. Hebbar, and T. Heulin. 1997. A simple method for the isolation of Azospirillum strains associated with the rhizosphere of rice. Can. J. Microbiol. 43:486-490.
62. Vanbleu, E., K. Marchal, M. Lambrecht, J. Mathys, and J. Vanderleyden. 2004. Annotation of the pRhico plasmid of Azospirillum brasilense reveals its role in determining the outer surface composition. FEMS Microbiol. Lett. 232:165-172.
63. Vial, L., C. Lavire, P. Mavingui, D. Blaha, J. Haurat, Y. Moënne-Loccoz, R. Bally, and F. Wisniewski-Dyé. 2006. Phase variation and genomic architecture changes in Azospirillum. J. Bacteriol. 188:5364-5373.
64. Vieille, C., and C. Elmerich. 1990. Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to Rhizobium meliloti nodPQ. Mol. Plant-Microbe Interact. 3:389-400.
65. Weinbauer, M. G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-181.
66. Wommack, K. E., and R. R. Colwell. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69-114.
67. Zdobnov, E. M., and R. Apweiler. 2001. InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848.