Diversity and evolution of the Phenazine Biosynthesis Pathways

Applied and Environmental Microbiology

Volumn 76, Issue 3, 2010, Pages 866-879

  Mavrodi, Dmitri V ^a   Peever, Tobin L ^a   Mavrodi, Olga V ^a   Parejko, James A ^a   Raaijmakers, Jos M ^b   Lemanceau, Philippe ^c   Mazurier, Sylvie ^c   Heide, Lutz ^d   Blankenfeldt, Wulf ^e   Weller, David M ^a   Thomashow, Linda S ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c CMSE   (France)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL CONTROLS; BIOSYNTHESIS PATHWAYS; BREVIBACTERIUM; BURKHOLDERIA; CEREAL CROP; COMMERCIAL FARMS; GENOME ANALYSIS; HORIZONTAL GENE TRANSFER; PLANT PATHOGEN; PSEUDOMONAS SPP; SECONDARY METABOLITES; SOIL-DWELLING; WASHINGTON STATE;

BACTERIA; BACTERIOLOGY; BIOCHEMISTRY; BIOSYNTHESIS; DNA SEQUENCES; GENE TRANSFER; GENES; INTELLIGENT VEHICLE HIGHWAY SYSTEMS; METABOLITES; SOILS;

MAGNETIC FIELD EFFECTS;

ANTIFUNGAL AGENT; BACTERIAL DNA; BACTERIAL PROTEIN; PHENAZINE DERIVATIVE;

BACTERIUM; BIOCONTROL AGENT; BIOLOGICAL CONTROL; GENE; GENETIC ANALYSIS; GENOME; PATHOGENICITY; SECONDARY METABOLITE;

ARTICLE; BACTERIAL GENE; BACTERIUM; BIOSYNTHESIS; CLASSIFICATION; DNA SEQUENCE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HORIZONTAL GENE TRANSFER; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT; PSEUDOMONAS; SEQUENCE ALIGNMENT; UNITED STATES;

ANTIFUNGAL AGENTS; BACTERIA; BACTERIAL PROTEINS; BASE SEQUENCE; BIOSYNTHETIC PATHWAYS; DNA, BACTERIAL; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENOTYPE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHENAZINES; PHYLOGENY; PLANTS; PSEUDOMONAS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; WASHINGTON;

BACTERIA (MICROORGANISMS); BREVIBACTERIUM; BURKHOLDERIA; PECTOBACTERIUM; PSEUDOMONAS; STREPTOMYCES;

EID: 75749090020     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02009-09     Document Type: Article

References (67)

1. Abken, H. J., M. Tietze, J. Brodersen, S. Baumer, U. Beifuss, and U. Deppenmeier. 1998. Isolation and characterization, of methanophenazine and function of phenazlnes in membrane-bound electron transport of Methanosarcina mazei Gol. J. Bacteriol. 180:2027-2032.
2. Ahuja, E. G., P. Janning, M. Mentel, A. Graebsch, R. Breinbauer, W. Hiller, B. Costisella, L. S. Thomashow, D. V. Mavrodi, and W. Blankenfeldt. 2008. PhzA/B catalyzes the formation of the tricycle in phenazine biosynthesis. J. Am. Chem.. Soc. 130:17053-17061.
3. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Automat. Control 19:716-723.
4. Anzai, Y., H. Kim, J. Y. Park, H. Wakabayashi, and H. Oyaizu. 2000. Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int. J. Syst. Evol. Microbiol. 50:1563-1589.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and S. K. 2002. Short protocols in molecular biology, 5th ed. John Wiley and Sons, New York, NY.
6. Axelrood, P. E., M. Relia, and M. N. Schroth. 1988. Role of antibiosis in competition of Erwinia strains in potato Infection courts. Appl. Environ. Microbiol. 54:1222-1229.
7. Bell, K. S., M. Sebaihia, L. Pritchard, M. T. Holden, L. J. Hyman, M. C. Holeva, N. R. Thomson, S. D. Bentley, L. J. Churcher, K. Mungall, R. Atkin, N. Bason, K. Brooks, T. Chillingworth, K. Clark, J. Doggett, A. Fraser, Z. Hance, H. Hauser, K. Jagels, S. Moule, H. Norbertczak, D. Ormond, C. Price, M. A. Quail, M. Sanders, D. Walker, S. Whitehead, G. P. Salmond, P. R. Birch, J. Parkhill, and I. K. Toth. 2004. Genome sequence of the enterobacterial phytopathogen. Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc. Natl. Acad. Sci. U. S. A. 101: 11105-11110.
8. Bennett-Lovsey, R. M., A. D. Herbert, M. J. Sternberg, and L. A. Kelley. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70:611-625.
9. Blankenfeldt, W., A. P. Kuzin, T. Skarina, Y. Korniyenko, L. Tong, P. Bayer, P. Janning, L. S. Thomashow, and D. V. Mavrodi. 2004. Structure and function of the phenazine biosynthetic protein PhzF from Pseudomonas fluoresces. Proc. Natl. Acad. Sci. U. S. A. 101:16431-16436.
10. Bull, C. T., C. A. Ishimaru, and J. E. Loper. 1994. Two genomic regions involved in catechol siderophore production by Erwinia carotovora. Appl. Environ. Microbiol. 60:662-669.
11. Cartwright, D. K., W. S. Chilton, and D. M. Benson. 1995. Pyrrolnitrin and phenazine production by Pseudomonas cepacia strain 5.5B, a biocontrol agent of Rhizoctonia solani. Appl. Microbiol. Biotechnol. 43:211-216.
12. Carver, T. J., K. M. Rutherford, M. Berriman, M. A. Rajandream, B. G. Barrell, and J. Parkhill. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
13. Chin-A-Woeng, T. F. C., G. V. Bloemberg, I. H. M. Mulders, L. C. Dekkers, and B. J. J. Lugtenberg. 2000. Root colonization, by phenazine-,1-carboxamide- producing bacterium Pseudomonas chlororaphls PCL1391. is essential for biocontrol of tomato foot and root rot. Mol. Plant Microbe Interact. 13: 1340-1345.
14. Chin-A-Woeng, T. F. C., J. E. Thomus-Oates, B. J. J. Lugtenberg, and G. V. Bloemberg. 2001. Introduction of the phzH gene of Pseudomonas chlororaphis PCL.1391 extends the range of biocontrol ability of phenazine-l.-carboxylic acid-producing Pseudomonas spp. strains. Mol. Plant Microbe Interact. 14:1.006-1015.
15. Ciccarelli, F. D., T. Doerks, C. von Mering, C. J. Creevey, B. Snel, and P. Bork. 2006. Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283-1287.
16. Coenye, T., P. Vandamme, J. J. LiPuma, J. R. Govan, and E. Mahenthirallngam. 2003. Updated version of the Burkholderia cepacia complex experimental strain, panel. J. Clin. Microbiol. 41:2797-2798.
17. Dietrich, L. E., T. K. Teal, A. Price-Whelan, and D. K. Newman. 2008. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203-1206.
18. Dietrich, L. E. P., A. Price-Whelan, A. Petersen, M. Whiteley, and D. K. Newman. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeiuginosa. Mol. Microbiol. 61: 1308-1321.
19. Fitzpatrick, D. A. 2009. Lines of evidence for horizontal gene transfer of a phenazine producing Operon into multiple bacterial species. J. Mol. Evol. 68:171-185.
20. Georgakopoulos, D. G., M. Hendson, N. J. Panopoulos, and M. N. Schroth. 1994. Cloning of a phenazine biosynthetic locus of Pseudomonas aureofaciens PGS12 and analysis of its expression in. vitro with the ice nucleation reporter gene. Appl. Environ. Microbiol. 60:2931-2938.
21. Giddens, S. R., Y. J. Feng, and H. K. Mahanty. 2002. Characterization of a novel phenazine antibiotic gene cluster in Erwinia herbicola Eh1087. Mol. Microbiol. 45:769-783.
22. Giddens, S. R., G. J. Houliston, and H. K. Mahanty. 2003. The influence of antibiotic production and pre-emptive colonization on the population dynamics of Pantoea agglomerans (Erwinia herbicola) Eh 1087 and Erwinia amylovora in. planta. Environ. Microbiol. 5:1016-1021.
23. Haagen, Y. 2007. Molecular and biochemical analyses of biosynthesis of phenazine and furanonaphthoqulnone I in Streptomyces cinnamonensis DSM. 1042. Ph.D. thesis. Eberhard Karls University, Tubingen, Germany.
24. Haagen, Y., K. Gluck, K. Fay, B. Kammerer, B. Gust, and L. Heide. 2006. A gene cluster for prenylated naphthoquinone and prenylated phenazine biosynthesis in Streptomyces cinnamonensis DSM. 1042. Chembiochem 7:2016-2027.
25. Hall, B. G. 2004. Phylogenetic trees made easy: a how-to manual. Sinauer Associates, Sunderland, MA.
26. Hernandez, M. E., A. Kappler, and D. K. Newman. 2004. Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl. Environ. Microbiol. 70:921.-928.
27. Huelsenbeck, J. P., J. J. Bull, and C. W. Cunningham. 1996. Combining data in phylogenetic analysis. Trends Ecol. Evol. 11:152-158.
28. Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Baysian inference of phylogenetic trees. Bioinformatics 17:754-755.
29. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:275-282.
30. Kimura, M. .1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
31. King, E. O., M. K. Ward, and D. E. Raney. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Clin. Med. 44:301-307.
32. Kube, M., A. M. Migdoll, I. Muller, H. Kuhl, A. Beck, R. Reinhardt, and K. Gelder. 2008. The genome of Erwinia tasmaniensis strain Etl/99, a nonpathogenic bacterium, in the genus Erwinia. Environ. Microbiol. 10:22112222.
33. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigun, H. McWilliam, F. Valentin, I. M. Wallace, A. WiIm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
34. Larsen, G. Y., T. L. Stulí, and J. L. Burns. 1993. Marked phenotypic variability in Pseudomonas cepacia isolated from a patient with cystic fibrosis. J. Qin. Microbiol. 31:788-792.
35. Lau, G. W., H. M. Ran, F. S. Kong, D. J. Hassett, and D. Mavrodi. 2004. Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect. Immun. 72:4275-11278
36. Laursen, J. B., and J. Nielsen. 2004. Phenazine natural products: biosynthesis, synthetic analogues, and biological, activity. Chem. Rev. 104:1663-1685.
37. Lerat, E., and N. A. Moran. 2004. The evolutionary history of quorumsensing systems in bacteria. Mol. Biol. Evol. 21:903-913.
38. LiPuma, J. J. 2005. Update on the Burkhotderia cepacia complex. Curr. Opin. Pulm. Med. 11:528-533.
39. Maddula, V. S., E. A. Pierson, and L. S. Pierson III. 2008. Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on. biofilm formation and pathogen inhibition. J. Bacteriol. 190:2759-2766.
40. Mahojan-Miklos, S., M. W. Tan, L. G. Rahme, and F. M. Ausubel. 1999. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96:47-56.
41. Mahenthiralingam, E., T. Coenye, J. W. Chung, D. P. Speert, J. R. Govan, P. Taylor, and P. Vandamme. 2000. Diagnostically and experimentally useful panel, of strains from the Burkhotderia cepacia complex. J. Clin. Microbiol. 38:910-913.
42. Mavrodi, D. V., W. Blankenfeldt, and L. S. Thomashow. 2006. Phenazine compounds in fluorescent Pseudomonas spp.: biosynthesis and regulation. Annu. Rev. Phytopathol. 44:417-445.
43. Mavrodi, D. V., R. F. Bonsall, S. M. Delaney, M. J. Soule, G. Phillips, and L. S. Thomashow. 2001. Functional, analysis of genes for biosynthesis of pyocyanin and phenazine-l-carboxamide from Pseudomonas aeruginosa PAOl. J. Bacteriol. 183:6454-6465.
44. Mavrodi, D. V., V. N. Ksenzenko, R. F. Bonsall, R. J. Cook, A. M. Boronin, and L. S. Thomashow. 1998. A seven-gene locus for synthesis of phenazine1-carboxylic acid by Pseudomonas fiuorescens 2-79. J. Bacteriol. 180:25412548.
45. Mazurler, S., T. Corberand, P. Lemanceau, and J. M. Raaijmakers. 2009. Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J. 3:977-991.
46. Mazzola, M., R. J. Cook, L. S. Thomashow, D. M. Weiler, and L. S. Pierson. 1992. Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl. Environ. Microbiol. 58:2616-2624.
47. McAlpine, J. B., A. H. Banskota, R. D. Charan, G. Schlingmann, E. Zazopoulos, M. Piraee, J. Janso, V. S. Bernan, M. Aouidate, C. M. Farnet, X. Feng, Z. Zhao, and G. T. Carter. 2008. Biosynthesis of diazepinomicin/ECO4601, a Micromonospora secondary metabolite with a novel ring system. J. Nat. Prod. 71:1585-1590.
48. McDonald, M., D. V. Mavrodi, L. S. Thomashow, and H. G. Floss. 2001. Phenazine biosynthesis in Pseudomonas fiuorescens: branchpoint from the primary shikimate biosynthetic pathway and role of phenazine-l,6-dicarboxylic acid. J. Am. Chem. Soc. 123:9459-9460.
49. Perneel, M., J. Heyrman, A. Adiobo, K. De Maeyer, J. M. Raajjmakers, P. De Vos, and M. Hofte. 2007. Characterization of CMR5c and CMR12a, novel fluorescent Pseudomonas strains from, the cocoyam rhizosphere with biocontrol activity. J. Appl. Microbiol. 103:1007-1020.
50. Pierson, L. S., T. Gaffney, S. Lam, and F. C. Gong. 1995. Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacterium Pseudomonas aureofaciens 30-84. FEMS Microbiol. Lett. 134:299-307.
51. 51. Posada, D. 2006. ModelTest Server: a web-based tool for the statistical selection, of models of nucleotide substitution online. Nucleic Acids Res. 34:W700-W703. (Pubitemid 44529861)
52. Price, E. W., and I. Carbone. 2005. SNAP: workbench management tool, for evolutionary population genetic analysis. Bioinformatics 21:402-404.
53. Price-Whelan, A., L. E. Dietrich, and D. K. Newman. 2006. Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2:71-78.
54. Rahme, L. G., F. M. Ausubel, H. Cao, E. Drenkard, B. C. Goumnerov, G. W. Lau, S. Mahajan-Miklos, J. Plotnikova, M. W. Tan, J. Tsongalis, C. L. Walendziewicz, and R. G. Tompkins. 2000. Plauts and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. U. S. A. 97:8815-8821.
55. Saleh, O., B. Gust, B. Boll, H. P. Fiedler, and L. Heide. 2009. Aromatic prenylation in phenazine biosynthesis: dihydrophenazine-1-carboxylate dim- ethylallyltransferase from Streptomyces anulatus. J. Biol. Chem. 284:1443914447.
56. Seo, S. T., and K. Tsuchiya. 2004. PCR-based identification and characterization of Burkholderia cepacia complex bacteria from, clinical and environmental sources. Lett. Appl. Microbiol. 39:413-419.
57. Shimodnira, H., and M. Hasegawa. 1999. Multiple comparisons of loglikelihoods with applications to phylogenetic inference. MoI. Biol. Evol. 16:1114-1116.
58. Stanier, R. Y., N. J. Palleroni, and M. Doudoroff. 1966. The aerobic pseudomonads: a taxonomie study. J. Gen. Microbiol. 43:159-271.
59. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PAOl, an opportunistic pathogen. Nature 406:959-964.
60. Swoffbrd, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (* and other methods), 4.Ob10 ed. Sinauer Associates, Sunderland, MA.
61. 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.
62. Thomashow, L. S., and D. M. Weiler. 1988. Role of a phenazine antibiotic from Pseudomonas fiuorescens in biological, control of Gaeumannomyces graminis var. tritici. J. Bacteriol. 170:3499-3508.
63. Thomashow, L. S., D. M. Weiler, R. F. Bonsall, and L. S. Pierson. 1990. Production of the antibiotic phenazine-1-carboxylic acid by fluorescent Pseudomonas species in the rhizosphere of wheat. Appl. Environ. Microbiol. 56:908-912.
64. Turner, J. M., and A. J. Messenger. 1986. Occurrence, biochemistry and physiology of phenazine pigment production. Adv. Microb. Physiol. 27:211275.
65. Vanlaere, E., A. Baldwin, D. Gevers, D. Henry, E. De Brandt, J. J. LiPuma, E. Mnhenthiralingam, D. P. Speert, C. Dowson, and P. Vandamme. 2009. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminons sp. nov. and Burkholderia lata sp. nov. Int. J. Syst. Evol. Microbiol. 59:102-111.
66. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697703.
67. Weiler, D. M. 1983. Colonization of wheat roots by a fluorescent pseudomonad suppressive to take-all. Phytopathology 73:1548-1553.