Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype

Genetics

Volumn 173, Issue 2, 2006, Pages 515-526

  Goymer, Patrick ^a   Kahn, Sophie G ^a   Malone, Jacob G ^b   Gehrig, Stefanie M ^a   Spiers, Andrew J ^a   Rainey, Paul B ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN WSPR; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; EVOLUTION; GENE IDENTIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; GENOTYPE; MICROBIAL DIVERSITY; MUTAGENESIS; NONHUMAN; PHENOTYPE; POPULATION GENETICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PSEUDOMONAS FLUORESCENS;

ALLELES; BACTERIAL PROTEINS; CELLULOSE; CONSERVED SEQUENCE; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHOSPHORYLATION; PSEUDOMONAS FLUORESCENS; SIGNAL TRANSDUCTION;

PSEUDOMONAS; PSEUDOMONAS FLUORESCENS;

EID: 33745402876     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.055863     Document Type: Article

References (60)

1. AGUILAR, P. S., A. M. HERNANDEZ-ARRIAGA, L. E. CYBULSKI, A. C. ERAZO and D. DE MENDOZA, 2001 Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J. 20: 1681-1691.
2. ALDRIDGE, P., R. PAUL, P. GOYMER, P. B. RAINEY and U. JENAL, 2003 Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol. Microbiol. 47: 1695-1708.
3. ALFANO, J. R., D. W. BAUER, T. M. MILOS and A. COLLMER, 1996 Analysis of the role of the Pseudomonas syringae pv syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally non-polar hrpZ deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol. Microbiol. 19: 715-728.
4. BAIKALOV, I., I. SCHRODER, M. KACZOR-GRZESKOWIAK, K. GRZESKOWIAK, R. P. GUNSALUS et al., 1996 Structure of the Escherichia coli response regulator NarL. Biochemistry 35: 11053-11061.
5. BANTINAKI, E., 2002 Characterization of a novel chemosensory pathway underlying adaptive evolution in experimental population of Pseudomonas fluorescens SBW25. Ph. D. Thesis, University of Oxford, Oxford.
6. BULL, J. J., M. R. BADGETT, H. A. WICHMAN, J. P. HUELSENBECK, D.M. HILLIS et al., 1997 Exceptional convergent evolution in a virus. Genetics 147: 1497-1507.
7. CHAMNONGPOL, S., and E. A. GROISMAN, 2000 Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase. J. Mol. Biol. 300: 291-305.
8. CHAN, C., R. PAUL, D. SAMORAY, N. C. AMIOT, B. GIESE et al., 2004 Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. USA 101: 17084-17089.
9. COOPER, T. F., D. E. ROZEN and R. E. LENSKI, 2003 Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl. Acad. Sci. USA 100: 1072-1077.
10. COOPER, V. S., D. SCHNEIDER, M. BLOT and R. E. LENSKI, 2001 Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacteriol. 183: 2834-2841.
11. CROZAT, E., N. PHILIPPE, R. E. LENSKI, J. GEISELMANN and D. SCHNEIDER, 2005 Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169: 523-532.
12. D'ARGENIO, D. A., M. W. CALFEE, P. B. RAINEY and E. C. PESCI, 2002 Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184: 6481-6489.
13. DA RE, S., T. TOLSTYKH, P. M. WOLANIN and J. B. STOCK, 2002 Genetic analysis of response regulator activation in bacterial chemotaxis suggests an intermolecular mechanism. Protein Sci. 11: 2644-2654.
14. DARWIN, C., 1890 The Origin of Species. John Murray, London.
15. DE ROSA, R., J. K. GRENIER, T. ANDREEVA, C. E. COOK, A. ADOUTTE et al., 1999 Hox genes in brachiopods and priapulids and protostome evolution. Nature 399: 772-776.
16. DJORDJEVIC, S., and A. M. STOCK, 1998 Structural analysis of bacterial chemotaxis proteins: Components of a dynamic signaling system. J. Struct. Biol. 124: 189-200.
17. DOBZHANSKY, T., 1951 Genetics and the Origin of Species. Columbia University Press, New York.
18. DOEBLEY, J., A. STEC and L. HUBBARD, 1997 The evolution of apical dominance in maize. Nature 386: 485-488.
19. FIGURSKI, D. H., and D. R. HELINSKI, 1979 Replication of an origin-containing derivative of plasmid RK2 dependant on a plasmid function supplied in trans. Proc. Natl. Acad. Sci. USA 76: 1648-1652.
20. GALPERIN, M. Y., 2004 Bacterial signal transduction network in a genomic perspective. Env. Microbiol. 6: 552-567.
21. GALPERIN, M. Y., A. N. NIKOLSKAYA and E. V. KOONIN, 2001 Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203: 11-21.
22. GEHRIG, S. M., 2005 Adaptation of Pseudomonas fluorescens SBW25 to the air-liquid interface: a study in evolutionary genetics. Ph. D. Thesis, University of Oxford, Oxford.
23. GERHART, J., and M. KIRSCHNER, 1997 Cells, Embryos, and Evolution. Blackwell, Malden, MA.
24. HICKMAN, J. W., D. F. TIFREA and C. S. HARWOOD, 2005 A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA 102: 14422-14427.
25. HOCH, J. A., and T. J. SILHAVY (Editors), 1995 Two-Component Signal Transduction. ASM Press, Washington, DC.
26. HORTON, R. M., H. D. HUNT, S. N. HO, J. K. PULLEN and L. R. PEASE, 1989 Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
27. KING, E. O., M. K. WARD and D. C. RANEY, 1954 Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44: 301-307.
28. KIRILLINA, O., J. D. FETHERSTON, A. G. BOBROV, J. ABNEY and R. D. PERRY, 2004 HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol. Microbiol. 54: 75-88.
29. LACK, D., 1947 Darwin's Finches. Cambridge University Press, Cambridge, UK.
30. LEE, S. Y., H. S. CHO, J. G. PELTON, D. L. YAN, E. A. BERRY et al., 2001 Crystal structure of activated CheY - Comparison with other activated receiver domains. J. Biol. Chem. 276: 16425-16431.
31. LENSKI, R. E., M. R. ROSE, S. C. SIMPSON and S. C. TADLER, 1991 Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138: 1315-1341.
32. LOPER, J. E., and S. E. LINDOW, 1994 A biological sensor for iron available to bacteria in their habitats on plant-surfaces. Appl. Env. Microbiol. 60: 1934-1941.
33. MARIS, A. E., M. R. SAWAYA, M. KACZOR-GRZESKOWIAK, M. R. JARVIS, S. M. D. BEARSON et al., 2002 Dimerization allows DNA target site recognition by the NarL response regulator. Nature Struct. Biol. 9: 771-778.
34. MILLER, J., 1972 Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. ORR, H. A., 2005 The genetic theory of adaptation: a brief history. Nat. Rev. Genet. 6: 119-127.
36. PAUL, R., S. WEISER, N. C. AMIOT, C. CHAN, T. SCHIRMER et al., 2004 Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18: 715-727.
37. PEI, J. M., and N. V. GRISHIN, 2001 GGDEF domain is homologous to adenylyl cyclase. Proteins 42: 210-216.
38. POWELL, B. S., and C. I. KADO, 1990 Specific binding of VirG to the vir box requires a C-terminal domain and exhibits a minimum concentration threshold. Mol. Microbiol. 4: 2159-2166.
39. RAINEY, P. B., 1999 Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Env. Microbiol. 1: 243-257.
40. RAINEY, P. B., and M. J. BAILEY, 1996 Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Mol. Microbiol. 19: 521-533.
41. RAINEY, P. B., and K. RAINEY, 2003 Evolution of cooperation and conflict in experimental bacterial populations. Nature 425: 72-74.
42. RAINEY, P. B., and M. TRAVISANO, 1998 Adaptive radiation in a heterogeneous environment. Nature 394: 69-72.
43. ROBINSON, V. L., T. WU and A. M. STOCK, 2003 Structural analysis of the domain interface in DrrB, a response regulator of the OmpR/PhoB subfamily. J. Bacteriol. 185: 4186-4194.
44. ROMLING, U., M. GOMELSKY and M. Y. GALPERIN, 2005 C-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57: 629-639.
45. ROSS, P., H. WEINHOUSE, Y. ALONI, D. MICHAELI, P. OHANA et al., 1987 Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281.
46. RYJENKOV, D. A., M. TARUTINA, O. V. MOSKVIN and M. GOMELSKY, 2005 Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187: 1792-1798.
47. SAMBROOK, J., E. F. FRITSCH and T. MANIATIS, 1989 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. SCHLUTER, D., 2000 The Ecology of Adaptive Radiation. Oxford University Press, Oxford.
49. SIAM, R., and G. T. MARCZYNSKI, 2003 Glutamate at the phosphorylation site of response regulator CtrA provides essential activities without increasing DNA binding. Nucleic Acids Res. 31: 1775-1779.
50. SIMON, R., U. PRIEFER and A. PUHLER, 1983 A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnol. 1: 784-791.
51. SIMPSON, G. G., 1953 The Major Features of Evolution. Columbia University Press, New York.
52. SMITH, J. G., J. A. LATIOLAIS, G. P. GUANGA, J. D. PENNINGTON, R. E. SILVERSMITH et al., 2004 A search for amino acid substitutions that universally activate response regulators. Mol. Microbiol. 51: 887-901.
53. SPIERS, A. J., and P. B. RAINEY, 2005 The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity. Microbiology 151: 2829-2839.
54. SPIERS, A. J., S. G. KAHN, J. BOHANNON, M. TRAVISANO and P. B. RAINEY, 2002 Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161: 33-46.
55. SPIERS, A. J., J. BOHANNON, S. M. GEHRIG and P. B. RAINEY, 2003 Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol. Microbiol. 50: 15-27.
56. STOCK, A. M., V. L. ROBINSON and P. N. GOUDREAU, 2000 Two-component signal transduction. Annu. Rev. Biochem. 69: 183-215.
57. TAL, R., H. C. WONG, R. CALHOON, D. GELFAND, A. L. FEAR et al., 1998 Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J. Bacteriol. 180: 4416-4425.
58. TREVES, D. S., S. MANNING and J. ADAMS, 1998 Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol. Biol. Evol. 15: 789-797.
59. WEST-EBERHARD, M. J., 2003 Developmental Plasticity and Evolution. Oxford University Press, Oxford.
60. WICHMAN, H. A., M. R. BADGETT, L. A. SCOTT, C. M. BOULIANNE and J. J. BULL, 1999 Different trajectories of parallel evolution during viral adaptation. Science 285: 422-424.