An iron detection system determines bacterial swarming initiation and biofilm formation

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Lin, Chuan Sheng ^a   Tsai, Yu Huan ^a   Chang, Chih Jung ^a   Tseng, Shun Fu ^a   Wu, Tsung Ru ^a   Lu, Chia Chen ^b   Wu, Ting Shu ^c   Lu, Jang Jih ^c   Horng, Jim Tong ^a   Martel, Jan ^a   Ojcius, David M ^a,d   Lai, Hsin Chih ^a,c,e   Young, John D ^a,f,g  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d UNIVERSITY OF THE PACIFIC   (United States)

^e CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^f ROCKEFELLER UNIVERSITY   (United States)

^g MING CHI UNIVERSITY OF TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

2-ISOCYANO-6,7-DIHYDROXYCOUMARIN; BACTERIAL PROTEIN; COUMARIN DERIVATIVE; IRON;

BACTERIAL PHENOMENA AND FUNCTIONS; BIOFILM; BIOLOGICAL MODEL; FLAGELLUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SERRATIA MARCESCENS; SIGNAL TRANSDUCTION;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; BIOFILMS; COUMARINS; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; IRON; MODELS, BIOLOGICAL; SERRATIA MARCESCENS; SIGNAL TRANSDUCTION;

EID: 84995511086     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep36747     Document Type: Article

References (53)

1. Andrews, S. C., Robinson, A. K., Rodriguez-Quinones, F. Bacterial iron homeostasis. FEMS Microbiol Rev 27, 215-237 (2003).
2. Touati, D. Iron and oxidative stress in bacteria. Arch Biochem Biophys 373, 1-6 (2000).
3. Yeom, J., Imlay, J. A., Park, W. Iron homeostasis affects antibiotic-mediated cell death in Pseudomonas species. J Biol Chem 285, 22689-22695 (2010).
4. Marx, J. J. Iron and infection: competition between host and microbes for a precious element. Best Pract Res Clin Haematol 15, 411-426 (2002).
5. Braun, V., Hantke, K. Recent insights into iron import by bacteria. Curr Opin Chem Biol 15, 328-334 (2011).
6. Cornelis, P., Wei, Q., Andrews, S. C., Vinckx, T. Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 3, 540-549 (2011).
7. Troxell, B., Hassan, H. M. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 3, 59 (2013).
8. Verstraeten, N. et al. Living on a surface: swarming and biofilm formation. Trends Microbiol 16, 496-506 (2008).
9. Lewis, K. Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322, 107-131 (2008).
10. Hall-Stoodley, L., Costerton, J. W., Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95-108 (2004).
11. Kearns, D. B., Losick, R. Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 49, 581-590 (2003).
12. Butler, M. T., Wang, Q., Harshey, R. M. Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci USA 107, 3776-3781 (2010).
13. Lai, S., Tremblay, J., Deziel, E. Swarming motility: a multicellular behaviour conferring antimicrobial resistance. Environ Microbiol 11, 126-136 (2009).
14. Overhage, J., Bains, M., Brazas, M. D., Hancock, R. E. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190, 2671-2679 (2008).
15. Partridge, J. D., Harshey, R. M. Swarming: flexible roaming plans. J Bacteriol 195, 909-918 (2013).
16. Harshey, R. M. Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57, 249-273 (2003).
17. Kim, W., Surette, M. G. Metabolic differentiation in actively swarming Salmonella. Mol Microbiol 54, 702-714 (2004).
18. Givskov, M. et al. Two separate regulatory systems participate in control of swarming motility of Serratia liquefaciens MG1. J Bacteriol 180, 742-745 (1998).
19. Rather, P. N. Swarmer cell differentiation in Proteus mirabilis. Environ Microbiol 7, 1065-1073 (2005).
20. Van Houdt, R., Givskov, M., Michiels, C. W. Quorum sensing in Serratia. FEMS Microbiol Rev 31, 407-424 (2007).
21. Mukherjee, S. et al. Adaptor-mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation. Proc Natl Acad Sci USA 112, 250-255 (2015).
22. Inoue, T. et al. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J Bacteriol 189, 950-957 (2007).
23. Wang, Q., Frye, J. G., McClelland, M., Harshey, R. M. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol Microbiol 52, 169-187 (2004).
24. McCarter, L., Silverman, M. Iron regulation of swarmer cell differentiation of Vibrio parahaemolyticus. J Bacteriol 171, 731-736 (1989).
25. Matilla, M. A. et al. Temperature and pyoverdine-mediated iron acquisition control surface motility of Pseudomonas putida. Environ Microbiol 9, 1842-1850 (2007).
26. Wu, Y., Outten, F. W. IscR controls iron-dependent biofilm formation in Escherichia coli by regulating type I fimbria expression. J Bacteriol 191, 1248-1257 (2009).
27. Singh, P. K., Parsek, M. R., Greenberg, E. P., Welsh, M. J. A component of innate immunity prevents bacterial biofilm development. Nature 417, 552-555 (2002).
28. Banin, E., Vasil, M. L., Greenberg, E. P. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102, 11076-11081 (2005).
29. Wosten, M. M., Kox, L. F., Chamnongpol, S., Soncini, F. C., Groisman, E. A. A signal transduction system that responds to extracellular iron. Cell 103, 113-125 (2000).
30. Laub, M. T., Goulian, M. Specificity in two-component signal transduction pathways. Annu Rev Genet 41, 121-145 (2007).
31. Krell, T. et al. Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64, 539-559 (2010).
32. Lai, H. C. et al. The RssAB two-component signal transduction system in Serratia marcescens regulates swarming motility and cell envelope architecture in response to exogenous saturated fatty acids. J Bacteriol 187, 3407-3414 (2005).
33. Lin, C. S. et al. RssAB-FlhDC-ShlBA as a major pathogenesis pathway in Serratia marcescens. Infect Immun 78, 4870-4881 (2010).
34. Soo, P. C. et al. Regulation of swarming motility and flhDCSm expression by RssAB signaling in Serratia marcescens. J Bacteriol 190, 2496-2504 (2008).
35. Tsai, Y. H. et al. RssAB signaling coordinates early development of surface multicellularity in Serratia marcescens. PLoS One 6, e24154 (2011).
36. Wei, J. R. et al. Biochemical characterization of RssA-RssB, a two-component signal transduction system regulating swarming behavior in Serratia marcescens. J Bacteriol 187, 5683-5690 (2005).
37. Wyckoff, E. E., Mey, A. R., Leimbach, A., Fisher, C. F., Payne, S. M. Characterization of ferric and ferrous iron transport systems in Vibrio cholerae. J Bacteriol 188, 6515-6523 (2006).
38. Livak, K. J., Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2CT Method. Methods 25, 402-408 (2001).
39. Clarke, M. B., Hughes, D. T., Zhu, C., Boedeker, E. C., Sperandio, V. The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci USA 103, 10420-10425 (2006).
40. Stintzi, A. et al. Novel pyoverdine biosynthesis gene(s) of Pseudomonas aeruginosa PAO. Microbiology 142 (Pt 5), 1181-1190 (1996).
41. Clarke-Pearson, M. F., Brady, S. F. Paerucumarin, a new metabolite produced by the pvc gene cluster from Pseudomonas aeruginosa. J Bacteriol 190, 6927-6930 (2008).
42. Drake, E. J., Gulick, A. M. Three-dimensional structures of Pseudomonas aeruginosa PvcA and PvcB, two proteins involved in the synthesis of 2-isocyano-6, 7-dihydroxycoumarin. J Mol Biol 384, 193-205 (2008).
43. Qaisar, U. et al. The pvc operon regulates the expression of the Pseudomonas aeruginosa fimbrial chaperone/usher pathway (cup) genes. PLoS One 8, e62735 (2013).
44. Rowland, M. A., Deeds, E. J. Crosstalk and the evolution of specificity in two-component signaling. Proc Natl Acad Sci USA 111, 5550-5555 (2014).
45. Garcia, C. A., Alcaraz, E. S., Franco, M. A., Passerini de Rossi, B. N. Iron is a signal for Stenotrophomonas maltophilia biofilm formation, oxidative stress response, OMPs expression, and virulence. Front Microbiol 6, 926 (2015).
46. Mehi, O. et al. Perturbation of iron homeostasis promotes the evolution of antibiotic resistance. Mol Biol Evol 31, 2793-2804 (2014).
47. Skaar, E. P. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6, e1000949 (2010).
48. Visaggio, D. et al. Cell aggregation promotes pyoverdine-dependent iron uptake and virulence in Pseudomonas aeruginosa. Front Microbiol 6, 902 (2015).
49. Nishino, K. et al. Identification of the lipopolysaccharide modifications controlled by the Salmonella PmrA/PmrB system mediating resistance to Fe(III) and Al(III). Mol Microbiol 61, 645-654 (2006).
50. Sambrook, J., Maniatis, T., Fritsch, E. F. Molecular cloning: a laboratory manual, 2nd ed. (Cold Spring Harbor Laboratory, 1989).
51. Dietz, P., Gerlach, G., Beier, D. Identification of target genes regulated by the two-component system HP166-HP165 of Helicobacter pylori. J Bacteriol 184, 350-362 (2002).
52. Bustin, S. A. et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55, 611-622 (2009).
53. Schwyn, B., Neilands, J. B. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160, 47-56 (1987).