Light regulation of swarming motility in Pseudomonas syringae integrates signaling pathways mediated by a bacteriophytochrome and a LOV protein

mBio

Volumn 4, Issue 3, 2013, Pages

  Wu, Liang ^a   McGrane, Regina S ^a   Beattie, Gwyn A ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIOPHYTOCHROME 1; BACTERIOPHYTOCHROME 2; LIGHT OXYGEN VOLTAGE PROTEIN; PHYTOCHROME; PROTEIN HISTIDINE KINASE; UNCLASSIFIED DRUG; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BLUE LIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; EPISTASIS; GENE DELETION; GENETIC COMPLEMENTATION; MUTATIONAL ANALYSIS; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; SWARMING MOTILITY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; LOCOMOTION; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RADIATION RESPONSE;

BACTERIA (MICROORGANISMS); PSEUDOMONAS SYRINGAE;

BACTERIAL PROTEINS; DNA MUTATIONAL ANALYSIS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; LIGHT; LOCOMOTION; PROTEIN KINASES; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION;

EID: 84879588276     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00334-13     Document Type: Article

References (53)

1. Kiang NY, Siefert J, Govindjee, Blankenship RE. 2007. Spectral signatures of photosynthesis. I. Review of Earth organisms. Astrobiology 7:222-251.
2. Kyndt JA, Meyer TE, Cusanovich MA. 2004. Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria. Photochem. Photobiol. Sci. 3:519-530.
3. Lin C, Shalitin D. 2003. Cryptochrome structure and signal transduction. Annu. Rev. Plant Biol. 54:469-496.
4. Jung A, Domratcheva T, Tarutina M, Wu Q, Ko WH, Shoeman RL, Gomelsky M, Gardner KH, Schlichting I. 2005. Structure of a bacterial BLUF photoreceptor: insights into blue light-mediated signal transduction. Proc. Natl. Acad. Sci. U. S. A. 102:12350-12355.
5. Swartz TE, Tseng TS, Frederickson MA, Paris G, Comerci DJ, Rajashekara G, Kim JG, Mudgett MB, Splitter GA, Ugalde RA, Goldbaum FA, Briggs WR, Bogomolni RA. 2007. Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317:1090-1093.
6. Metz S, Haberzettl K, Frühwirth S, Teich K, Hasewinkel C, Klug G. 2012. Interaction of two photoreceptors in the regulation of bacterial photosynthesis genes. Nucleic Acids Res. 40:5901-5909.
7. Demba Diallo M, Monteil CL, Vinatzer BA, Clarke CR, Glaux C, Guilbaud C, Desbiez C, Morris CE. 2012. Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic. ISME J. 6:1325-1335.
8. Bhoo SH, Davis SJ, Walker J, Karniol B, Vierstra RD. 2001. Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414:776-779.
9. Gomelsky M, Hoff WD. 2011. Light helps bacteria make important lifestyle decisions. Trends Microbiol. 19:441-448.
10. Smith H. 2000. Phytochromes and light signal perception by plants-an emerging synthesis. Nature 407:585-591.
11. Yeh KC, Wu SH, Murphy JT, Lagarias JC. 1997. A cyanobacterial phytochrome two-component light sensory system. Science 277: 1505-1508.
12. Shah R, Schwach J, Frankenberg-Dinkel N, Gärtner W. 2012. Complex formation between heme oxygenase and phytochrome during biosynthesis in Pseudomonas syringae pv. tomato. Photochem. Photobiol. Sci. 11: 1026-1031.
13. Kojadinovic M, Laugraud A, Vuillet L, Fardoux J, Hannibal L, Adriano JM, Bouyer P, Giraud E, Verméglio A. 2008. Dual role for a bacteriophytochrome in the bioenergetic control of Rhodopseudomonas palustris: enhancement of photosystem synthesis and limitation of respiration. Biochim. Biophys. Acta 1777:163-172.
14. Giraud E, Fardoux J, Fourrier N, Hannibal L, Genty B, Bouyer P, Dreyfus B, Verméglio A. 2002. Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417:202-205.
15. Giraud E, Zappa S, Vuillet L, Adriano JM, Hannibal L, Fardoux J, Berthomieu C, Bouyer P, Pignol D, Verméglio A. 2005. A new type of bacteriophytochrome acts in tandem with a classical bacteriophytochrome to control the antennae synthesis in Rhodopseudomonas palustris. J. Biol. Chem. 280:32389-32397.
16. Fiedler B, Broc D, Schubert H, Rediger A, Börner T, Wilde A. 2004. Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem. Photobiol. 79:551-555.
17. Wilde A, Fiedler B, Börner T. 2002. The cyanobacterial phytochrome Cph2 inhibits phototaxis towards blue light. Mol. Microbiol. 44:981-988.
18. Fiedler B, Börner T, Wilde A. 2005. Phototaxis in the cyanobacterium Synechocystis sp. PCC 6803: role of different photoreceptors. Photochem. Photobiol. 81:1481-1488.
19. Terauchi K, Montgomery BL, Grossman AR, Lagarias JC, Kehoe DM. 2004. RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol. Microbiol. 51: 567-577.
20. Yoshihara S, Ikeuchi M. 2004. Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochem. Photobiol. Sci. 3:512-518.
21. Ikeuchi M, Ishizuka T. 2008. Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in Cyanobacteria. Photochem. Photobiol. Sci. 7:1159-1167.
22. Davis SJ, Vener AV, Vierstra RD. 1999. Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286:2517-2520.
23. Barkovits K, Schubert B, Heine S, Scheer M, Frankenberg-Dinkel N. 2011. Function of the bacteriophytochrome BphP in the RpoS/las quorum-sensing network of Pseudomonas aeruginosa. Microbiology (Reading, Engl.) 157:1651-1664.
24. Karniol B, Vierstra RD. 2003. The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc. Natl. Acad. Sci. U. S. A. 100:2807-2812.
25. Oberpichler I, Rosen R, Rasouly A, Vugman M, Ron EZ, Lamparter T. 2008. Light affects motility and infectivity of Agrobacterium tumefaciens. Environ. Microbiol. 10:2020-2029.
26. Briggs WR. 2007. The LOV domain: a chromophore module servicing multiple photoreceptors. J. Biomed. Sci. 14:499-504.
27. Jentzsch K, Wirtz A, Circolone F, Drepper T, Losi A, Gärtner W, Jaeger KE, Krauss U. 2009. Mutual exchange of kinetic properties by extended mutagenesis in two short LOV domain proteins from Pseudomonas putida. Biochemistry 48:10321-10333.
28. Crosson S, Rajagopal S, Moffat K. 2003. The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42:2-10.
29. Herrou J, Crosson S. 2011. Function, structure and mechanism of bacterial photosensory LOV proteins. Nat. Rev. Microbiol. 9:713-723.
30. Cao Z, Buttani V, Losi A, Gärtner W. 2008. A blue light inducible two-component signal transduction system in the plant pathogen Pseudomonas syringae pv. tomato. Biophys. J. 94:897-905.
31. Kraiselburd I, Alet AI, Tondo ML, Petrocelli S, Daurelio LD, Monzón J, Ruiz OA, Losi A, Orellano EG. 2012. A LOV protein modulates the physiological attributes of Xanthomonas axonopodis pv. citri relevant for host plant colonization. PLoS One 7:e38226. http://dx.doi.org/10.1371/journal.pone.0038226.
32. Purcell EB, Siegal-Gaskins D, Rawling DC, Fiebig A, Crosson S. 2007.A photosensory two-component system regulates bacterial cell attachment. Proc. Natl. Acad. Sci. U. S. A. 104:18241-18246.
33. Bonomi HR, Posadas DM, Paris G, del Carmen Carrica M, Frederickson M, Pietrasanta LI, Bogomolni RA, Zorreguieta A, Goldbaum FA. 2012. Light regulates attachment, exopolysaccharide production, and nodulation in Rhizobium leguminosarum through a LOV-histidine kinase photoreceptor. Proc. Natl. Acad. Sci. U. S. A. 109:12135-12140.
34. Patrick JE, Kearns DB. 2012. Swarming motility and the control of master regulators of flagellar biosynthesis. Mol. Microbiol. 83:14-23.
35. Burch AY, Shimada BK, Mullin SW, Dunlap CA, Bowman MJ, Lindow SE. 2012. Pseudomonas syringae coordinates production of a motilityenabling surfactant with flagellar assembly. J. Bacteriol. 194:1287-1298.
36. Alteri CJ, Himpsl SD, Engstrom MD, Mobley HL. 2012. Anaerobic respiration using a complete oxidative TCA cycle drives multicellular swarming in Proteus mirabilis. mBio 3(6):e00365-12. http://dx.doi.org/10.1128/mBio.00365-12.
37. Merritt JH, Brothers KM, Kuchma SL, O'Toole GA. 2007. SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J. Bacteriol. 189:8154-8164.
38. Chow S, Gu K, Jiang L, Nassour A. 2011. Salicylic acid affects swimming, twitching and swarming motility in Pseudomonas aeruginosa, resulting in decreased biofilm formation. J. Exp. Microbiol. Immunol. 15:22-29.
39. Heeb S, Itoh Y, Nishijyo T, Schnider U, Keel C, Wade J, Walsh U, O'Gara F, Haas D. 2000. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Mol. Plant Microbe Interact. 13:232-237.
40. Wright CA, Beattie GA. 2004. Bacterial species specificity in proU osmoinducibility and nptII and lacZ expression. J. Mol. Microbiol. Biotechnol. 8:201-208.
41. Castillon A, Shen H, Huq E. 2009. Blue light induces degradation of the negative regulator phytochrome interacting factor 1 to promote photomorphogenic development of Arabidopsis seedlings. Genetics 182: 161-171.
42. Franklin KA, Larner VS, Whitelam GC. 2005. The signal transducing photoreceptors of plants. Int. J. Dev. Biol. 49:653-664.
43. Ahmad M, Jarillo JA, Smirnova O, Cashmore AR. 1998. The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Mol. Cell 1:939-948.
44. Mas P, Devlin PF, Panda S, Kay SA. 2000. Functional interaction of phytochrome B and cryptochrome 2. Nature 408:207-211.
45. Han IS, Tseng TS, Eisinger W, Briggs WR. 2008. Phytochrome A regulates the intracellular distribution of phototropin 1-green fluorescent protein in Arabidopsis thaliana. Plant Cell 20:2835-2847.
46. Yanovsky MJ, Casal JJ, Luppi JP. 1997. The VLF loci, polymorphic between ecotypes Landsberg erecta and Columbia, dissect two branches of phytochrome A signal transduction that correspond to very-low-fluence and high-irradiance responses. Plant J. 12:659-667.
47. Hockett KL, Burch AY, Lindow SE. 2013. Thermo-regulation of genesmediating motility and plant interactions in Pseudomonas syringae. PLoS One 8:e59850. http://dx.doi.org/10.1371/journal.pone.0059850.
48. Loper JE, Lindow SE. 1987. Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathology 77:1449-1454.
49. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
50. Chen C, Malek AA, Wargo MJ, Hogan DA, Beattie GA. 2010. The ATP-binding cassette transporter Cbc (choline/betaine/carnitine) recruits multiple substrate-binding proteins with strong specificity for distinct quaternary ammonium compounds. Mol. Microbiol. 75:29-45.
51. Figurski DH, Helinski DR. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652.
52. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
53. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.