Vibrio cholerae NspS, a homologue of ABC-type periplasmic solute binding proteins, facilitates transduction of polyamine signals independent of their transport

Microbiology (United Kingdom)

Volumn 160, Issue PART 5, 2014, Pages 832-843

  Cockerell, Steven R ^a   Rutkovsky, Alex C ^b   Zayner, Josiah P ^c   Cooper, Rebecca E ^d   Porter, Lindsay R ^e   Pendergraft, Sam S ^f   Parker, Zach M ^g   McGinnis, Marcus W ^h   Karatan, Ece ⁱ  

^a Old Hickory Brewery   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^e Woodward Academy   (United States)

^f WAKE FOREST UNIVERSITY   (United States)

^g Dartmouth College   (United States)

^h SYNGENTA BIOTECHNOLOGY INC   (United States)

ⁱ APPALACHIAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; NORSPERMIDINE; NSPS PROTEIN; PERIPLASMIC BINDING PROTEIN; PHOSPHODIESTERASE; POLYAMINE; SPERMIDINE; SPERMIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; CONTROLLED STUDY; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOBACTERIA; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

EID: 84899139714     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.075903-0     Document Type: Article

References (44)

1. Bomchil, N., Watnick, P. & Kolter, R. (2003). Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J Bacteriol 185, 1384-1390.
2. Burrell, M., Hanfrey, C. C., Murray, E. J., Stanley-Wall, N. R. & Michael, A. J. (2010). Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation. J Biol Chem 285, 39224-39238.
3. Christensen, H., Bertelsen, M. F., Bojesen, A. M. & Bisgaard, M. (2012). Classification of Pasteurella species B as Pasteurella oralis sp. nov. Int J Syst Evol Microbiol 62, 1396-1401.
4. Datsenko, K. A. & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640-6645.
5. Davidson, A. L., Dassa, E., Orelle, C. & Chen, J. (2008). Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72, 317-364.
6. Eym, Y., Park, Y. & Park, C. (1996). Genetically probing the regions of ribose-binding protein involved in permease interaction. Mol Microbiol 21, 695-702.
7. Gardina, P., Conway, C., Kossman, M. & Manson, M. (1992). Aspartate and maltose-binding protein interact with adjacent sites in the Tar chemotactic signal transducer of Escherichia coli. J Bacteriol 174, 1528-1536.
8. Gillespie, J. J., Wattam, A. R., Cammer, S. A., Gabbard, J. L., Shukla, M. P., Dalay, O., Driscoll, T., Hix, D., Mane, S. P. & other authors (2011). PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect Immun 79, 4286-4298.
9. Giuliani, S. E., Frank, A. M. & Collart, F. R. (2008). Functional assignment of solute-binding proteins of ABC transporters using a fluorescence-based thermal shift assay. Biochemistry 47, 13974-13984.
10. Goytia, M., Dhulipala, V. L. & Shafer, W. M. (2013). Spermine impairs biofilm formation by Neisseria gonorrhoeae. FEMS Microbiol Lett 343, 64-69.
11. Hamana, K. (1997). Polyamine distribution patterns within the families Aeromonadaceae, Vibrionaceae, Pasteurellaceae, and Halomonadaceae, and related genera of the gamma subclass of the Proteobacteria. J Gen Appl Microbiol 43, 49-59.
12. Hamana, K. & Itoh, T. (2001). Polyamines of the hyperthermophilic archaebacteria belonging to the genera Thermococcus and Methanothermus and two new genera Caldivirga and Palaeococcus. Microbios 104, 105-114.
13. Hamana, K., Niitsu, M., Samejima, K. & Matsuzaki, S. (1991). Novel tetraamines, pentaamines and hexaamines in sea-urchin, sea-cucumber, sea squirt and bivalves. Comp Biochem Physiol B 100, 59-62.
14. Hamana, K., Niitsu, M. & Samejima, K. (1998). Unusual polyamines in aquatic plants: the occurrence of homospermidine, norspermidine, thermospermine, norspermine, aminopropylhomospermidine, bis(aminopropyl) ethanediamine, and methylspermidine. Can J Bot 76, 130-133.
15. Hamana, K., Niitsu, M., Samejima, K. & Itoh, T. (2001). Polyamines of the thermophilic eubacteria belonging to the genera Thermosipho, Thermaerobacter and Caldicellulosiruptor. Microbios 104, 177-185.
16. Hamana, K., Aizaki, T., Arai, E., Saito, A., Uchikata, K. & Ohnishi, H. (2004). Distribution of norspermidine as a cellular polyamine within micro green algae including non-photosynthetic achlorophyllous Polytoma, Polytomella, Prototheca and Helicosporidium. J Gen Appl Microbiol 50, 289-295.
17. Haugo, A. J. & Watnick, P. I. (2002). Vibrio cholerae CytR is a repressor of biofilm development. Mol Microbiol 45, 471-483.
18. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. & Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
19. Hu, X., Zhao, J., DeGrado, W. F. & Binns, A. N. (2013). Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals. Proc Natl Acad Sci U S A 110, 678-683.
20. Igarashi, K. & Kashiwagi, K. (2010). Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42, 39-51.
21. Karatan, E., Duncan, T. R. & Watnick, P. I. (2005). NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J Bacteriol 187, 7434-7443.
22. Kashiwagi, K., Hosokawa, N., Furuchi, T., Kobayashi, H., Sasakawa, C., Yoshikawa, M. & Igarashi, K. (1990). Isolation of polyamine transport-deficient mutants of Escherichia coli and cloning of the genes for polyamine transport proteins. J Biol Chem 265, 20893-20897.
23. Kashiwagi, K., Pistocchi, R., Shibuya, S., Sugiyama, S., Morikawa, K. & Igarashi, K. (1996). Spermidine-preferential uptake system in Escherichia coli. Identification of amino acids involved in polyamine binding in PotD protein. J Biol Chem 271, 12205-12208.
24. Keating, T. A., Marshall, C. G. & Walsh, C. T. (2000). Vibriobactin biosynthesis in Vibrio cholerae: VibH is an amide synthase homologous to nonribosomal peptide synthetase condensation domains. Biochemistry 39, 15513-15521.
25. Kolodkin-Gal, I., Cao, S., Chai, L., Böttcher, T., Kolter, R., Clardy, J. & Losick, R. (2012). A self-produced trigger for biofilm disassembly that targets exopolysaccharide. Cell 149, 684-692.
26. Lee, J., Sperandio, V., Frantz, D. E., Longgood, J., Camilli, A., Phillips, M. A. & Michael, A. J. (2009). An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae. J Biol Chem 284, 9899-9907.
27. McGinnis, M. W., Parker, Z. M., Walter, N. E., Rutkovsky, A. C., Cartaya-Marin, C. & Karatan, E. (2009). Spermidine regulates Vibrio cholerae biofilm formation via transport and signaling pathways. FEMS Microbiol Lett 299, 166-174.
28. Metcalf, W. W., Jiang, W., Daniels, L. L., Kim, S. K., Haldimann, A. & Wanner, B. L. (1996). Conditionally replicative and conjugative plasmids carrying lacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35, 1-13.
29. Miller, V. L. & Mekalanos, J. J. (1988). A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170, 2575-2583.
30. Neiditch, M. B., Federle, M. J., Miller, S. T., Bassler, B. L. & Hughson, F. M. (2005). Regulation of LuxPQ receptor activity by the quorumsensing signal autoinducer-2. Mol Cell 18, 507-518.
31. Ni, S., Forouhar, F., Bussiere, D. E., Robinson, H. & Kennedy, M. A. (2006). Crystal structure of VC0702 at 2. 0 Å: conserved hypothetical protein from Vibrio cholerae. Proteins 63, 733-741.
32. Niesen, F. H., Berglund, H. & Vedadi, M. (2007). The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2, 2212-2221.
33. Parker, Z. M., Pendergraft, S. S., Sobieraj, J., McGinnis, M. M. & Karatan, E. (2012). Elevated levels of the norspermidine synthesis enzyme NspC enhance Vibrio cholerae biofilm formation without affecting intracellular norspermidine concentrations. FEMS Microbiol Lett 329, 18-27.
34. Patel, C. N., Wortham, B. W., Lines, J. L., Fetherston, J. D., Perry, R. D. & Oliveira, M. A. (2006). Polyamines are essential for the formation of plague biofilm. J Bacteriol 188, 2355-2363.
35. Römling, U., Galperin, M. Y. & Gomelsky, M. (2013). Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77, 1-52.
36. Ryjenkov, D. A., Tarutina, M., Moskvin, O. V. & Gomelsky, M. (2005). Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187, 1792-1798.
37. Shilton, B. H., Flocco, M. M., Nilsson, M. & Mowbray, S. L. (1996). Conformational changes of three periplasmic receptors for bacterial chemotaxis and transport: the maltose-, glucose/galactose-and ribose-binding proteins. J Mol Biol 264, 350-363.
38. Tabor, C. W. & Tabor, H. (1984). Polyamines. Annu Rev Biochem 53, 749-790.
39. Tan, K., Chang, C., Cuff, M., Osipiuk, J., Landorf, E., Mack, J. C., Zerbs, S., Joachimiak, A. & Collart, F. R. (2013). Structural and functional characterization of solute binding proteins for aromatic compounds derived from lignin: p-coumaric acid and related aromatic acids. Proteins 81, 1709-1726.
40. Trimble, M. J. & McCarter, L. L. (2011). Bis-(39-59)-cyclic dimeric GMP-linked quorum sensing controls swarming in Vibrio parahaemolyticus. Proc Natl Acad Sci U S A 108, 18079-18084.
41. Ulijasz, A. T., Grenader, A. & Weisblum, B. (1996). A vancomycininducible lacZ reporter system in Bacillus subtilis: induction by antibiotics that inhibit cell wall synthesis and by lysozyme. J Bacteriol 178, 6305-6309.
42. Waldor, M. K. & Mekalanos, J. J. (1994). Emergence of a new cholera pandemic: molecular analysis of virulence determinants in Vibrio cholerae O139 and development of a live vaccine prototype. J Infect Dis 170, 278-283.
43. 1-acetylnorspermidine in Vibrio parahaemolyticus and an enzyme activity responsible for its formation. FEMS Microbiol Lett 61, 225-230.
44. Zhao, J. & Binns, A. N. (2011). Characterization of the mmsAB-araD1 (gguABC) genes of Agrobacterium tumefaciens. J Bacteriol 193, 6586-6596.