Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus

PLoS Pathogens

Volumn 8, Issue 2, 2012, Pages

  Hobley, Laura ^a   Fung, Rowena K Y ^a   Lambert, Carey ^a   Harris, Maximilian A T S ^a   Dabhi, Jayesh M ^b   King, Simon S ^a   Basford, Sarah M ^a   Uchida, Kaoru ^c   Till, Robert ^a   Ahmad, Rashidah ^a   Aizawa, Shin Ichi ^c   Gomelsky, Mark ^b   Sockett, R Elizabeth ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF WYOMING   (United States)

^c PREFECTURAL UNIVERSITY OF HIROSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; CYCLIC DI GUANOSINE MONOPHOSPHATE; CYCLIC GMP; DIGUANYLATE CYCLASE; GLYCYLGLYCYLALANYLALANYLPHENYLALANINE; GLYCYLGLYCYLASPARTYLGLUTAMYLPHENYLALANINE; GUANYLATE CYCLASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BIS(3',5') CYCLIC DIGUANYLIC ACID; BIS(3',5')-CYCLIC DIGUANYLIC ACID; DRUG DERIVATIVE; ESCHERICHIA COLI PROTEIN; LYASE;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERIUM MUTANT; BACTERIUM PREDATION; BDELLOVIBRIO; BDELLOVIBRIO BACTERIOVORUS; CELL MOTILITY; ENZYME ACTIVITY; GENE DELETION; GENE FUNCTION; GENE INACTIVATION; NERVE FIBER GROWTH; NONHUMAN; PHENOTYPE; PREDATION; PREDATOR PREY INTERACTION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; WILD TYPE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOGENICITY;

ANIMALIA; BACTERIA (MICROORGANISMS); BDELLOVIBRIO; BDELLOVIBRIO BACTERIOVORUS; NEGIBACTERIA; PROTEOBACTERIA;

BACTERIAL PROTEINS; BDELLOVIBRIO; CYCLIC GMP; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; PHOSPHORUS-OXYGEN LYASES; SIGNAL TRANSDUCTION;

EID: 84860905515     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002493     Document Type: Article

References (50)

1. Lambert C, Evans KJ, Till R, Hobley L, Capeness M, et al. (2006) Characterizing the flagellar filament and the role of motility in bacterial prey-penetration by Bdellovibrio bacteriovorus. Mol Microbiol 60: 274-286.
2. Lambert C, Fenton AK, Hobley L, Sockett RE, (2011) Predatory Bdellovibrio Bacteria Use Gliding Motility to Scout for Prey on Surfaces. J Bacteriol 193: 3139-3141.
3. Dashiff A, Junka RA, Libera M, Kadouri DE, (2011) Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. J Appl Microbiol 110: 431-444.
4. Jurkevitch E, Minz D, Ramati B, Barel G, (2000) Prey range characterization, ribotyping, and diversity of soil and rhizosphere Bdellovibrio spp. isolated on phytopathogenic bacteria. Appl Environ Microbiol 66: 2365-2371.
5. Sockett RE, Lambert C, (2004) Bdellovibrio as therapeutic agents: a predatory renaissance? Nat Rev Microbiol 2: 669-675.
6. Fenton AK, Kanna M, Woods RD, Aizawa S-I, Sockett RE, (2010) Shadowing the actions of a predator: backlit fluorescent microscopy reveals synchronous nonbinary septation of predatory Bdellovibrio inside prey and exit through discrete bdelloplast pores. J Bacteriol 192: 6329-6335.
7. Horowitz AT, Kessel M, Shilo M, (1974) Growth cycle of predacious Bdellovibrios in a host-free extract system and some properties of the host extract. J Bacteriol 117: 270-282.
8. Thomashow LS, Rittenberg SC, (1985) Isolation and composition of sheathed flagella from Bdellovibrio bacteriovorus 109J. J Bacteriol 163: 1047-1054.
9. Barel G, Jurkevitch E, (2001) Analysis of phenotypic diversity among host-independent mutants of Bdellovibrio bacteriovorus 109J. Arch Microbiol 176: 211-216.
10. Roschanski N, Klages S, Reinhardt R, Linscheid M, Strauch E, (2011) Identification of Genes Essential for Prey-Independent Growth of Bdellovibrio bacteriovorus HD100. J Bacteriol 193: 1745-1756.
11. Hengge R, (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
12. Wolfe AJ, Visick KL, (2010) The second messenger cyclic di-GMP. Washington, DC ASM Press.
13. Tamayo R, Pratt JT, Camilli A, (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61: 131-148.
14. Gomelsky M, (2011) cAMP, c-di-GMP, c-di-AMP and now cGMP: Bacteria use them all! Mol Microbiol 79: 562-565.
15. Chan C, Paul R, Samoray D, Amiot NC, Giese B, et al. (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101: 17084-17089.
16. Amikam D, Galperin MY, (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 3-6.
17. Galperin MY, (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6: 552-567.
18. Galperin MY, Higdon R, Kolker E, (2010) Interplay of heritage and habitat in the distribution of bacterial signal transduction systems. Mol Biosyst 6: 721-728.
19. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.
20. Schirmer T, Jenal U, (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7: 724-735.
21. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, et al. (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303: 689-692.
22. Pallen M, Chaudhuri R, Khan A, (2002) Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol 10: 556-563.
23. Ko M, Park C, (2000) Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J Mol Biol 303: 371-382.
24. Ryjenkov DA, Simm R, Romling U, Gomelsky M, (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J Biol Chem 281: 30310-30314.
25. De N, Pirruccello M, Krasteva PV, Bae N, Raghavan RV, et al. (2008) Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLosONE 6: e67.
26. Ryjenkov DA, Simm R, Römling U, Gomelsky M, (2006) The PilZ domain is a receptor for the second messenger c-di-GMP. J Biol Chem 281: 30310-30314.
27. Steyert SR, Pineiro SA, (2007) Development of a novel genetic system to create markerless deletion mutants of Bdellovibrio bacteriovorus. Appl Environ Microbiol 73: 4717-4724.
28. Iida Y, Hobley L, Lambert C, Fenton AK, Sockett RE, et al. (2009) Roles of multiple flagellins in flagellar formation and flagellar growth post bdelloplast lysis in Bdellovibrio bacteriovorus. J Mol Biol 394: 1011-1021.
29. Lambert C, Smith MC, Sockett RE, (2003) A novel assay to monitor predator-prey interactions for Bdellovibrio bacteriovorus 109 J reveals a role for methyl-accepting chemotaxis proteins in predation. Environ Microbiol 5: 127-132.
30. Cotter TW, Thomashow MF, (1992) Identification of a Bdellovibrio bacteriovorus genetic locus, hit, associated with the host-independent phenotype. J Bacteriol 174: 6018-6024.
31. Bobrov AG, Kirillina O, Ryjenkov DA, Waters CM, Price PA, et al. (2011) Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol Microbiol 79: 533-551.
32. Hickman JW, Tifrea DF, Harwood CS, (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102: 14422-14427.
33. Hickman JW, Harwood CS, (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376-389.
34. Kadouri D, O'Toole GA, (2005) Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microbiol 71: 4044-4051.
35. Wurtzel O, Dori-Bachash M, Pietrokovski S, Jurkevitch E, Sorek R, (2010) Mutation detection with next-generation resequencing through a mediator genome. PLosONE 5: e15628.
36. Galperin MY, (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5: 35.
37. Solano C, Garcia B, Latasa C, Toledo-Arana A, Zorraquino V, et al. (2009) Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc Natl Acad Sci U S A 106: 7997-8002.
38. Gomelsky M, (2009) The core pathway: diguanylate cyclases, phosphodiesterases, and c-di-GMP-binding proteins. In: Wolfe A, Visick K, editors. The second messenger cyclic di-GMP Washington, DC ASM Press pp. 37-56.
39. Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, et al. (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23: 93-104.
40. Guvener ZT, Harwood CS, (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66: 1459-1473.
41. Merritt JH, Ha DG, Cowles KN, Lu W, Morales DK, et al. (2010) Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases. MBio 19: e00183-10.
42. Kuchma SL, Ballok AE, Merritt JH, Hammond JH, Lu W, et al. (2010) Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J Bacteriol 192: 2950-2964.
43. Simm R, Lusch A, Kader A, Andersson M, Romling U, (2007) Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J Bacteriol 189: 3613-3623.
44. Morehouse KA, Hobley L, Capeness M, Sockett RE, (2011) Three motAB Stator Gene Products in Bdellovibrio bacteriovorus Contribute to Motility of a Single Flagellum during Predatory and Prey-Independent Growth. J Bacteriol 193: 932-943.
45. Evans KJ, Lambert C, Sockett RE, (2007) Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J Bacteriol 189: 4850-4859.
46. Roschanski N, Klages S, Reinhardt R, Linscheid M, Strauch E, (2011) Identification of genes essential for prey independent growth of Bdellovibrio bacteriovorus HD100. J Bacteriol 193: 1745-1756.
47. Lambert C, Chang CY, Capeness MJ, Sockett RE, (2010) The first bite-profiling the predatosome in the bacterial pathogen Bdellovibrio. PLoS One 5: e8599.
48. Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M, (2005) Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: Insights into the biochemistry of the GGDEF protein domain. J Bacteriol 187: 1792-1798.
49. Fenton AK, Lambert C, Wagstaff PC, Sockett RE, (2010) Manipulating each MreB of Bdellovibrio bacteriovorus gives diverse morphological and predatory phenotypes. J Bacteriol 192: 1299-1311.
50. De N, Navarro MV, Raghavan RV, Sondermann H, (2009) Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J Mol Biol 393: 619-633.