1887

Abstract

The polyamines norspermidine and spermidine are among the environmental signals that regulate biofilm formation. The effects of these polyamines are mediated by NspS, a member of the bacterial periplasmic solute binding protein superfamily. Almost all members of this superfamily characterized to date are components of ATP-binding cassette-type transporters involved in nutrient uptake. Consequently, in the current annotation of the genome, NspS has been assigned a function in transport. The objective of this study was to further characterize NspS and investigate its potential role in transport. Our results support a role for NspS in signal transduction in response to norspermidine and spermidine, but not their transport. In addition, we provide evidence that these polyamine signals are processed by c-di-GMP signalling networks in the cell. Furthermore, we present comparative genomics analyses which reveal the presence of NspS-like proteins in a variety of bacteria, suggesting that periplasmic ligand binding proteins may be widely utilized for sensory transduction.

Funding
This study was supported by the:
  • Appalachian State University Department of Biology
  • Office of Student Research and the Graduate Student Association
  • Senate at Appalachian State University
  • University Research Council
  • National Institute of Allergy and Infectious Disease
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.075903-0
2014-05-01
2021-05-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/5/832.html?itemId=/content/journal/micro/10.1099/mic.0.075903-0&mimeType=html&fmt=ahah

References

  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  10. Goytia M., Dhulipala V. L., Shafer W. M. ( 2013). Spermine impairs biofilm formation by Neisseria gonorrhoeae. FEMS Microbiol Lett 343:64–69 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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
    [Google Scholar]
  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
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  17. Haugo A. J., Watnick P. I. ( 2002). Vibrio cholerae CytR is a repressor of biofilm development. Mol Microbiol 45:471–483 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  20. Igarashi K., Kashiwagi K. ( 2010). Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42:39–51 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  30. Neiditch M. B., Federle M. J., Miller S. T., Bassler B. L., Hughson F. M. ( 2005). Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 18:507–518 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  38. Tabor C. W., Tabor H. ( 1984). Polyamines. Annu Rev Biochem 53:749–790 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  40. Trimble M. J., McCarter L. L. ( 2011). Bis-(3′-5′)-cyclic dimeric GMP-linked quorum sensing controls swarming in Vibrio parahaemolyticus. Proc Natl Acad Sci U S A 108:18079–18084 [CrossRef][PubMed]
    [Google Scholar]
  41. Ulijasz A. T., Grenader A., Weisblum B. ( 1996). A vancomycin-inducible lacZ reporter system in Bacillus subtilis: induction by antibiotics that inhibit cell wall synthesis and by lysozyme. J Bacteriol 178:6305–6309[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  43. Yamamoto S., Nakao H., Koumoto Y., Shinoda S. ( 1989). Identification of N1-acetylnorspermidine in Vibrio parahaemolyticus and an enzyme activity responsible for its formation. FEMS Microbiol Lett 61:225–230 [CrossRef][PubMed]
    [Google Scholar]
  44. Zhao J., Binns A. N. ( 2011). Characterization of the mmsAB-araD1 (gguABC) genes of Agrobacterium tumefaciens. J Bacteriol 193:6586–6596 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.075903-0
Loading
/content/journal/micro/10.1099/mic.0.075903-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error