Requirement of polyphosphate by Pseudomonas fluorescens Pf0-1 for competitive fitness and heat tolerance in laboratory media and sterile soil

Applied and Environmental Microbiology

Volumn 75, Issue 12, 2009, Pages 3872-3881

  Silby, Mark W ^a   Nicoll, Julie S ^a   Levy, Stuart B ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID STRESS; ANTISENSE RNA; BIOLOGICAL CONTROLS; BROTH CULTURE; COMPETITIVE FITNESS; CRITICAL COMPONENT; ELEVATED TEMPERATURE; GENETIC BASIS; HEAT TOLERANCE; INORGANIC PHOSPHATES; LOAM SOILS; POLYPHOSPHATE; PSEUDOMONAS FLUORESCENS; SOIL ENVIRONMENT; STERILE SOIL; WILD TYPES;

BACTERIOLOGY; GENETIC ENGINEERING; HEALTH; NUCLEIC ACIDS; PLANTS (BOTANY); RNA; STRATEGIC PLANNING;

SOILS;

COMPLEMENTARY RNA; PHOSPHATE; PHOSPHOTRANSFERASE; POLYPHOSPHATE KINASE; UNCLASSIFIED DRUG;

BACTERIUM; BIOLOGICAL CONTROL; ENZYME ACTIVITY; FITNESS; GENETIC ANALYSIS; LABORATORY METHOD; LOAM; MUTATION; PHOSPHATE; RNA; SOIL MICROORGANISM; SURVIVAL; TEMPERATURE TOLERANCE;

ACIDITY; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; GENE LOCUS; HEAT TOLERANCE; LOAM SOIL; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PROTEIN EXPRESSION; PSEUDOMONAS FLUORESCENS; REGULON; TEMPERATURE SENSITIVITY;

ACIDS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE ORDER; HOT TEMPERATURE; OSMOTIC PRESSURE; OXIDATIVE STRESS; PHOSPHOTRANSFERASES (PHOSPHATE GROUP ACCEPTOR); POLYPHOSPHATES; PSEUDOMONAS FLUORESCENS; REGULON; RNA, ANTISENSE; SOIL MICROBIOLOGY; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS); PSEUDOMONAS FLUORESCENS;

EID: 67149100891     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00017-09     Document Type: Article

References (48)

1. Ault-Riche, D., C. D. Fraley, C.-M. Tzeng, and A. Kornberg. 1998. Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J. Bacteriol. 180:1841-1847. (Pubitemid 28173065)
2. Bertani, I., M. Scaronevo, M. Kojic, and V. Venturi. 2003. Role of GacA, LasI, RhlI, Ppk, PsrA, Vfr and ClpXP in the regulation of the stationaryphase sigma factor rpoS/RpoS in Pseudomonas. Arch. Microbiol. 180:264-271. (Pubitemid 37260454)
3. Camilli, A., and J. J. Mekalanos. 1995. Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol. Microbiol. 18:671-683.
4. Candon, H. L., B. J. Allan, C. D. Fraley, and E. C. Gaynor. 2007. Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. J. Bacteriol. 189:8099-8108.
5. Compeau, G., B. J. Al-Achi, E. Platsouka, and S. B. Levy. 1988. Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl. Environ. Microbiol. 54:2432-2438.
6. Deflaun, M. F., A. S. Tanzer, A. L. McAteer, B. Marshall, and S. B. Levy. 1990. Development of an adhesion assay and characterization of an adhesion-deficient mutant of Pseudomonas fluorescens. Appl. Environ. Microbiol. 56:112-119.
7. Fraley, C. D., M. H. Rashid, S. S. K. Lee, R. Gottschalk, J. Harrison, P. J. Wood, M. R. W. Brown, and A. Kornberg. 2007. A polyphosphate kinase 1 (ppk1) mutant of Pseudomonas aeruginosa exhibits multiple ultrastructural and functional defects. Proc. Natl. Acad. Sci. USA 104:3526-3531.
8. Gal, M., G. M. Preston, R. C. Massey, A. J. Spiers, and P. B. Rainey. 2003. Genes encoding a cellulosic polymer contribute toward the ecological success of Pseudomonas fluorescens SBW25 on plant surfaces. Mol. Ecol. 12:3109-3121.
9. Ghorbel, S., A. Smirnov, H. Chouayekh, B. Sperandio, C. Esnault, J. Kormanec, and M.-J. Virolle. 2006. Regulation of ppk expression and in vivo function of Ppk in Streptomyces lividans TK24. J. Bacteriol. 188:6269-6276.
10. Haas, D., and G. Defago. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319.
11. 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. (Pubitemid 19125654)
12. Jahid, I. K., A. J. Silva, and J. A. Benitez. 2006. Polyphosphate stores enhance the ability of Vibrio cholerae to overcome environmental stresses in a low-phosphate environment. Appl. Environ. Microbiol. 72:7043-7049.
13. Kato, J., T. Yamamoto, K. Yamada, and H. Ohtake. 1993. Cloning, sequence and characterization of the polyphosphate kinase-encoding gene (ppk) of Klebsiella aerogenes. Gene 137:237-242. (Pubitemid 24071640)
14. Kim, H. J., K. Y. Yang, B. H. Cho, K. Y. Kim, M. C. Lee, Y. H. Kim, A. J. Anderson, and Y. C. Kim. 2007. Transcript accumulation from the rpoS gene encoding a stationary-phase sigma factor in Pseudomonas chlororaphis strain O6 is regulated by the polyphosphate kinase gene. Curr. Microbiol. 54:219-223.
15. Kim, K.-S., N. N. Rao, C. D. Fraley, and A. Kornberg. 2002. Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc. Natl. Acad. Sci. USA 99:7675-7680. (Pubitemid 34568750)
16. Kim, W., and S. B. Levy. 2008. Increased fitness of Pseudomonas fluorescens Pf0-1 leucine auxotrophs in soil. Appl. Environ. Microbiol. 74:3644-3651.
17. Kirner, S., S. Krauss, G. Sury, S. T. Lam, J. M. Ligon, and K. H. vanPee. 1996. The non-haem chloroperoxidase from Pseudomonas fluorescens and its relationship to pyrrolnitrin biosynthesis. Microbiology 142:2129-2135.
18. Kornberg, A., N. N. Rao, and D. Ault-Riche. 1999. Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68:89-125.
19. Lowe, A. M., D. T. Beattie, and R. L. Deresiewicz. 1998. Identification of novel staphylococcal virulence genes by in vivo expression technology. Mol. Microbiol. 27:967-976.
20. Mahan, M. J., J. M. Slauch, and J. J. Mekalanos. 1993. Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259:686-688. (Pubitemid 23066292)
21. Marshall, B., E. A. Robleto, R. Wetzler, P. Kulle, P. Casaz, and S. B. Levy. 2001. The adnA transcriptional factor affects persistence and spread of Pseudomonas fluorescens under natural field conditions. Appl. Environ. Microbiol. 67:852-857.
22. Maurhofer, M., C. Reimmann, P. Schmidli-Sacherer, S. Heeb, D. Haas, and G. Defago. 1998. Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88:678-684.
23. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Monds, R. D., P. D. Newell, R. H. Gross, and G. A. O'Toole. 2007. Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol. 63:656-679.
25. Monds, R. D., P. D. Newell, J. A. Schwartzman, and G. A. O'Toole. 2006. Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Appl. Environ. Microbiol. 72:1910-1924.
26. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
27. Ogawa, N., C.-M. Tzeng, C. D. Fraley, and A. Kornberg. 2000. Inorganic polyphosphate in Vibrio cholerae: genetic, biochemical, and physiologic features. J. Bacteriol. 182:6687-6693.
28. Rainey, P. B. 1999. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1:243-257.
29. Rainey, P. B., and G. M. Preston. 2000. In vivo expression technology strategies: valuable tools for biotechnology. Curr. Opin. Biotechnol. 11:440-444.
30. Rao, N. N., and A. Kornberg. 1996. Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J. Bacteriol. 178:1394-1400. (Pubitemid 26073397)
31. Rao, N. N., S. Liu, and A. Kornberg. 1998. Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J. Bacteriol. 180:2186-2193.
32. Rashid, M. H., and A. Kornberg. 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 97:4885-4890.
33. Rashid, M. H., N. N. Rao, and A. Kornberg. 2000. Inorganic polyphosphate is required for motility of bacterial pathogens. J. Bacteriol. 182:225-227. (Pubitemid 30004581)
34. Rashid, M. H., K. Rumbaugh, L. Passador, D. G. Davies, A. N. Hamood, B. H. Iglewski, and A. Kornberg. 2000. Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 97:9636-9641.
35. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Seufferheld, M. J., H. M. Alvarez, and M. E. Farias. 2008. Role of polyphosphates in microbial adaptation to extreme environments. Appl. Environ. Microbiol. 74:5867-5874.
37. Shi, X., N. N. Rao, and A. Kornberg. 2004. Inorganic polyphosphate in Bacillus cereus: motility, biofilm formation, and sporulation. Proc. Natl. Acad. Sci. USA 101:17061-17065.
38. Shiba, T., K. Tsutsumi, H. Yano, Y. Ihara, A. Kameda, K. Tanaka, H. Takahashi, M. Munekata, N. N. Rao, and A. Kornberg. 1997. Inorganic polyphosphate and the induction of rpoS expression. Proc. Natl. Acad. Sci. USA 94:11210-11215.
39. Silby, M. W., and S. B. Levy. 2008. Overlapping protein-encoding genes in Pseudomonas fluorescens Pf0-1. PLoS Genet. 4:e1000094.
40. Silby, M. W., and S. B. Levy. 2004. Use of in vivo expression technology to identify genes important in growth and survival of Pseudomonas fluorescens Pf0-1 in soil: discovery of expressed sequences with novel genetic organization. J. Bacteriol. 186:7411-7419.
41. Simon, R., U. Priefer, and A. Puhler. 1983. A broad-host-range mobilization system for in vivo engineering: transposon mutagenesis in gram-negative bacteria. Bio/Technology 1:748-751.
42. 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 PA01, an opportunistic pathogen. Nature 406:959-964.
43. Sureka, K., S. Dey, P. Datta, A. K. Singh, A. Dasgupta, S. Rodrigue, J. Basu, and M. Kundu. 2007. Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol. Microbiol. 65:261-276.
44. van Veen, J. A., L. S. van Overbeek, and J. D. van Elsas. 1997. Fate and activity of microorganisms introduced into soil. Microbiol. Mol. Biol. Rev. 61:121-135.
45. Vessey, J. K. 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571-586. (Pubitemid 37417836)
46. Wanner, B. L. 1996. Phosphorus assimilation and control of the phosphate regulon, p. 1357-1381. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol.1. ASM Press, Washington, DC.
47. Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379-407.
48. Zhang, H., N. N. Rao, T. Shiba, and A. Kornberg. 2005. Inorganic polyphosphate in the social life of Myxococcus xanthus: motility, development, and predation. Proc. Natl. Acad. Sci. USA 102:13416-13420.