1887

Abstract

The surface layer (S-layer) protein genes of the uranium mining waste pile isolate JG-A12 and of its relative NCTC 9602 were analysed. The almost identical N-termini of the two S-layer proteins possess a unique structure, comprising three N-terminal S-layer homologous (SLH) domains. The central parts of the proteins share a high homology and are related to the S-layer proteins of CCM 2177 and P-1. In contrast, the C-terminal parts of the S-layer proteins of JG-A12 and NCTC 9602 differ significantly between each other. Surprisingly, the C-terminal part of the S-layer protein of JG-A12 shares a high identity with that of the S-layer protein of CCM 2177. In both JG-A12 and NCTC 9602 the chromosomal S-layer protein genes are followed by a newly identified putative insertion element comprising three ORFs, which encode a putative transposase, a putative integrase/recombinase and a putative protein containing a DNA binding helix–turn–helix motif, and the S-layer-protein-like gene copies (9602) or (JG-A12). Interestingly, both strains studied were found to contain an additional, plasmid-located and silent S-layer protein gene with the same sequence as and . The primary structures of the corresponding putative proteins are almost identical in both strains. The N-terminal and central parts of these S-layer proteins share a high identity with those of the chromosomally encoded functional S-layer proteins. Their C-terminal parts, however, differ significantly. These results strongly suggest that the S-layer protein genes have evolved via horizontal transfer of genetic information followed by DNA rearrangements mediated by mobile elements.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28201-0
2005-09-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/9/mic1512961.html?itemId=/content/journal/micro/10.1099/mic.0.28201-0&mimeType=html&fmt=ahah

References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G. & Struhl, K. ( 1993; ). Current Protocols in Molecular Biology. New York: Wiley.
  3. Bahl, H., Scholz, H., Bayan, N. & 27 other authors ( 1997; ). Molecular biology of S-layers. FEMS Microbiol Rev 20, 47–98.[CrossRef]
    [Google Scholar]
  4. Beuzon, C. R. & Casadesus, J. ( 1997; ). Conserved structure of IS200 elements in Salmonella. Nucleic Acids Res 25, 1355–1361.[CrossRef]
    [Google Scholar]
  5. Blaser, M. J., Wang, E., Tummuru, M. K., Washburn, R., Fujimoto, S. & Labigne, A. ( 1994; ). High-frequency S-layer protein variation in Campylobacter fetus revealed by sapA mutagenesis. Mol Microbiol 14, 453–462.[CrossRef]
    [Google Scholar]
  6. Boot, H. J. & Pouwels, P. H. ( 1996; ). Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol Microbiol 21, 1117–1123.[CrossRef]
    [Google Scholar]
  7. Boot, H. J., Kolen, C. P., Pot, B., Kersters, K. & Pouwels, P. H. ( 1996a; ). The presence of two S-layer-protein-encoding genes is conserved among species related to Lactobacillus acidophilus. Microbiology 142, 2375–2384.[CrossRef]
    [Google Scholar]
  8. Boot, H. J., Kolen, C. P. & Pouwels, P. H. ( 1996b; ). Interchange of the active and silent S-layer protein genes of Lactobacillus acidophilus by inversion of the chromosomal slp segment. Mol Microbiol 21, 799–809.[CrossRef]
    [Google Scholar]
  9. Borst, P. & Greaves, D. R. ( 1987; ). Programmed gene rearrangements altering gene expression. Science 235, 658–667.[CrossRef]
    [Google Scholar]
  10. Bowditch, R. D., Baumann, P. & Yousten, A. A. ( 1989; ). Cloning and sequencing of the gene encoding a 125-kilodalton surface-layer protein from Bacillus sphaericus 2362 and of a related cryptic gene. J Bacteriol 171, 4178–4188.
    [Google Scholar]
  11. Bravo, A. ( 1997; ). Phylogenetic relationships of Bacillus thuringiensis Δ-endotoxin family proteins and their functional domains. J Bacteriol 179, 2793–2801.
    [Google Scholar]
  12. Chan, E. C. S., Rutter, P. J. & Wills, A. ( 1973; ). Abundant growth and sporulation of Bacillus sphaericus NCA Hoop 1-A-2 in a chemically defined medium. Can J Microbiol 19, 151–154.[CrossRef]
    [Google Scholar]
  13. Cozzone, A. J. ( 1988; ). Protein phosphorylation in prokaryotes. Annu Rev Microbiol 42, 97–125.[CrossRef]
    [Google Scholar]
  14. Deblaere, R. Y., Desomer, J. & Dhaese, P. ( 1995; ). Expression of surface layer proteins. Patent no. WO9519371-A/8, 20-JUL-1995. EMBL AC no. A45814.
  15. Dworkin, J. & Blaser, M. J. ( 1996; ). Generation of Campylobacter fetus S-layer protein diversity utilizes a single promoter on an invertible DNA segment. Mol Microbiol 19, 1241–1253.[CrossRef]
    [Google Scholar]
  16. Dybvig, K. ( 1993; ). DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10, 465–471.[CrossRef]
    [Google Scholar]
  17. Egelseer, E. M., Schocher, I., Sára, M. & Sleytr, U. B. ( 1995; ). The S-layer from Bacillus stearothermophilus DSM 2358 functions as an adhesion site for a high-molecular-weight amylase. J Bacteriol 177, 1444–1451.
    [Google Scholar]
  18. Egelseer, E. M., Schocher, I., Sleytr, U. B. & Sára, M. ( 1996; ). Evidence that an N-terminal S-layer protein fragment triggers the release of a cell-associated high-molecular-weight amylase in Bacillus stearothermophilus ATCC 12980. J Bacteriol 178, 5602–5609.
    [Google Scholar]
  19. Egelseer, E. M., Idris, R., Jarosch, M., Danhorn, T., Sleytr, U. B. & Sára, M. ( 2000; ). ISBst12, a novel type of insertion-sequence element causing loss of S-layer-gene expression in Bacillus stearothermophilus ATCC 12980. Microbiology 146, 2175–2183.
    [Google Scholar]
  20. Engelhardt, H. & Peters, J. ( 1998; ). Structural research on surface layers: a focus on stability, surface layer homology domains, and surface layer-cell wall interactions. J Struct Biol 124, 276–302.[CrossRef]
    [Google Scholar]
  21. Gustafson, C. E., Chu, S. & Trust, T. J. ( 1994; ). Mutagenesis of the paracrystalline surface protein array of Aeromonas salmonicida by endogenous insertion elements. J Mol Biol 237, 452–463.[CrossRef]
    [Google Scholar]
  22. Hansmeier, N., Bartels, F. W., Ros, R. D. A., Tauch, A., Pühler, A. & Kalinowski, J. ( 2004; ). Classification of hyper-variable Corynebacterium glutamicum surface-layer proteins by sequence analyses and atomic force microscopy. J Biotechnol 112, 177–193.[CrossRef]
    [Google Scholar]
  23. Hastie, A. T. & Brinton, C. C. ( 1979a; ). Isolation, characterization, and in vitro assembly of the tetragonally arrayed layer of Bacillus sphaericus. J Bacteriol 138, 999–1009.
    [Google Scholar]
  24. Hastie, A. T. & Brinton, C. C. ( 1979b; ). Specific interactions of the tetragonally arrayed protein layer of Bacillus sphaericus with its peptidoglycan sacculus. J Bacteriol 138, 1010–1021.
    [Google Scholar]
  25. Hynönen, U., Westerlund-Wikstrom, B., Palva, A. & Korhonen, T. K. ( 2002; ). Identification by flagellum display of an epithelial cell- and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis. J Bacteriol 184, 3360–3367.[CrossRef]
    [Google Scholar]
  26. Ilk, N., Kosma, P., Puchberger, M., Egelseer, E. M., Mayer, H. F., Sleytr, U. B. & Sára, M. ( 1999; ). Structural and functional analyses of the secondary cell wall polymer of Bacillus sphaericus CCM 2177 that serves as an S-layer-specific anchor. J Bacteriol 181, 7643–7646.
    [Google Scholar]
  27. Ilk, N., Vollenkle, C., Egelseer, E. M., Breitwieser, A., Sleytr, U. B. & Sára, M. ( 2002; ). Molecular characterization of the S-layer gene, sbpA, of Bacillus sphaericus CCM 2177 and production of a functional S-layer fusion protein with the ability to recrystallize in a defined orientation while presenting the fused allergen. Appl Environ Microbiol 68, 3251–3260.[CrossRef]
    [Google Scholar]
  28. Ishiguro, E. E., Kay, W. W., Ainsworth, T., Chamberlain, J. B., Austen, R. A., Buckley, J. T. & Trust, T. J. ( 1981; ). Loss of virulence during culture of Aeromonas salmonicida at high temperature. J Bacteriol 148, 333–340.
    [Google Scholar]
  29. Jakava-Viljanen, M., Avall-Jaaskelainen, S., Messner, P., Sleytr, U. B. & Palva, A. ( 2002; ). Isolation of three new surface layer protein genes (slp) from Lactobacillus brevis ATCC 14869 and characterization of the change in their expression under aerated and anaerobic conditions. J Bacteriol 184, 6786–6795.[CrossRef]
    [Google Scholar]
  30. Kersulyte, D., Akopyants, N. S., Clifton, S. W., Roe, B. A. & Berg, D. E. ( 1998; ). Novel sequence organization and insertion specificity of IS605 and IS606: chimaeric transposable elements of Helicobacter pylori. Gene 223, 175–186.[CrossRef]
    [Google Scholar]
  31. Kersulyte, D., Mukhopadhyay, A. K., Shirai, M., Nakazawa, T. & Berg, D. E. ( 2000; ). Functional organization and insertion specificity of IS607, a chimeric element of Helicobacter pylori. J Bacteriol 182, 5300–5308.[CrossRef]
    [Google Scholar]
  32. Kuen, B., Sleytr, U. B. & Lubitz, W. ( 1994; ). Sequence analysis of the sbsA gene encoding the 130-kDa surface-layer protein of Bacillus stearothermophilus strain PV72. Gene 145, 115–120.[CrossRef]
    [Google Scholar]
  33. Kuen, B., Koch, A., Asenbauer, E., Sára, M. & Lubitz, W. ( 1997; ). Molecular characterization of the Bacillus stearothermophilus PV72 S-layer gene sbsB induced by oxidative stress. J Bacteriol 179, 1664–1670.
    [Google Scholar]
  34. Kyte, J. & Doolittle, R. F. ( 1982; ). A simple method for displaying the hydropathic character of a protein. J Mol Biol 157, 105–132.[CrossRef]
    [Google Scholar]
  35. Lam, S. & Roth, J. R. ( 1983a; ). Genetic mapping of IS200 copies in Salmonella typhimurim strain LT2. Genetics 105, 801–811.
    [Google Scholar]
  36. Lam, S. & Roth, J. R. ( 1983b; ). IS200: a Salmonella-specific insertion sequence. Cell 34, 951–960.[CrossRef]
    [Google Scholar]
  37. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  38. Lepault, J., Martin, N. & Leonard, K. ( 1986; ). Three-dimensional structure of the T-layer of Bacillus sphaericus P-1. J Bacteriol 168, 303–308.
    [Google Scholar]
  39. Lewis, L. O., Yousten, A. A. & Murray, R. G. ( 1987; ). Characterization of the surface protein layers of the mosquito-pathogenic strains of Bacillus sphaericus. J Bacteriol 169, 72–79.
    [Google Scholar]
  40. Luscombe, N. M., Austin, S. E., Berman, H. M. & Thornton, J. M. ( 2000; ). An overview of the structures of protein-DNA complexes. Genome Biol 1. doi:10.1186/gb-2000-1-1-reviews001
    [Google Scholar]
  41. Marchler-Bauer, A., Anderson, J. B., DeWeese-Scott, C. & 24 other authors ( 2003; ). CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31, 383–387.[CrossRef]
    [Google Scholar]
  42. Matuschek, M., Burchhardt, G., Sahm, K. & Bahl, H. ( 1994; ). Pullulanase of Thermoanaerobacterium thermosulfurigenes EM1 (Clostridium thermosulfurogenes): molecular analysis of the gene, composite structure of the enzyme, and a common model for its attachment to the cell surface. J Bacteriol 176, 3295–3302.
    [Google Scholar]
  43. Merroun, M., Raff, J., Rossberg, A., Hennig, C., Reich, T. & Selenska-Pobell, S. ( 2005; ). Complexation of uranium with S-layers of Bacillus sphaericus JG-A12 and NCTC 9602. Appl Environ Microbiol (in press).
    [Google Scholar]
  44. Mesnage, S., Haustant, M. & Fouet, A. ( 2001; ). A general strategy for identification of S-layer genes in the Bacillus cereus group: molecular characterization of such a gene in Bacillus thuringiensis subsp. galleriae NRRL 4045. Microbiology 147, 1343–1351.
    [Google Scholar]
  45. Mignot, T., Denis, B., Couture-Tosi, E., Kolsto, A. B., Mock, M. & Fouet, A. ( 2001; ). Distribution of S-layers on the surface of Bacillus cereus strains: phylogenetic origin and ecological pressure. Environ Microbiol 3, 493–501.[CrossRef]
    [Google Scholar]
  46. Mignot, T., Mesnage, S., Couture-Tosi, E., Mock, M. & Fouet, A. ( 2002; ). Developmental switch of S-layer protein synthesis in Bacillus anthracis. Mol Microbiol 43, 1615–1627.[CrossRef]
    [Google Scholar]
  47. Mignot, T., Mock, M. & Fouet, A. ( 2003; ). A plasmid-encoded regulator couples the synthesis of toxins and surface structures in Bacillus anthracis. Mol Microbiol 47, 917–927.[CrossRef]
    [Google Scholar]
  48. Miteva, V., Selenska-Pobell, S. & Mitev, V. ( 1999; ). Random and repetitive primer amplified polymorphic DNA analysis of Bacillus sphaericus. J Appl Microbiol 86, 928–936.[CrossRef]
    [Google Scholar]
  49. Murai, N., Kamata, H., Nagashima, Y., Yagisawa, H. & Hirata, H. ( 1995; ). A novel insertion sequence (IS)-like element of the thermophilic bacterium PS3 promotes expression of the alanine carrier protein-encoding gene. Gene 163, 103–107.[CrossRef]
    [Google Scholar]
  50. Ohnesorge, F., Heckl, W. M., Häberle, W. & 7 other authors ( 1992; ). Scanning force microscopy studies of the S-layers from Bacillus coagulans E38-66, Bacillus sphaericus CCM 2177, and of an antibody binding process. Ultramicroscopy 42–44, 1238–1242.
    [Google Scholar]
  51. Raff, J. ( 2002; ). Wechselwirkungen der Hüllproteine von Bakterien aus Uranabfallhalden mit Schwermetallen. PhD thesis, University of Leipzig. FZR-Report no. 358.
    [Google Scholar]
  52. Raff, J. & Selenska-Pobell, S. ( 2004; ). Posttranslational modifications of the S-layer protein from Bacillus sphaericus JG-A12 and its influence on uranium binding. FZR-Report no. 400.
    [Google Scholar]
  53. Raff, J., Merroun, M., Rossberg, A., Hennig, C. & Selenska-Pobell, S. ( 2003; ). EXAFS study of U(VI) complexes formed by native and recrystallized S-layers of Bacillus sphaericus JG-A12 and NCTC 9602. FZR-Report no. 373.
    [Google Scholar]
  54. Raff, J., Merroun, M., Rossberg, A., Soltmann, U. & Selenska-Pobell, S. ( 2004; ). Interactions of the U mining waste pile isolate Bacillus sphaericus JG-A12 with U. In Water–Rock Interaction, pp. 697–701. Edited by R. B. Wanty & R. R. Seal. London: Balkema Publishers.
  55. Sadowski, P. ( 1986; ). Site-specific recombinases: changing partners and doing the twist. J Bacteriol 165, 341–347.
    [Google Scholar]
  56. Saier, M. H., Jr, Wu, L. F. & Reizer, J. ( 1990; ). Regulation of bacterial physiological processes by three types of protein phosphorylating systems. Trends Biochem Sci 15, 391–395.[CrossRef]
    [Google Scholar]
  57. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  58. Sára, M. & Sleytr, U. B. ( 1987; ). Molecular sieving through S layers of Bacillus stearothermophilus strains. J Bacteriol 169, 4092–4098.
    [Google Scholar]
  59. Sára, M. & Sleytr, U. B. ( 2000; ). S-layer proteins. J Bacteriol 182, 859–868.[CrossRef]
    [Google Scholar]
  60. Scholz, H., Hummel, S., Witte, A., Lubitz, W. & Kuen, B. ( 2000; ). The transposable element IS4712 prevents S-layer gene (sbsA) expression in Bacillus stearothermophilus and also affects the synthesis of altered surface layer proteins. Arch Microbiol 174, 97–103.[CrossRef]
    [Google Scholar]
  61. Scholz, H. C., Riedmann, E., Witte, A., Lubitz, W. & Kuen, B. ( 2001; ). S-layer variation in Bacillus stearothermophilus PV72 is based on DNA rearrangements between the chromosome and the naturally occurring megaplasmids. J Bacteriol 183, 1672–1679.[CrossRef]
    [Google Scholar]
  62. Selenska-Pobell, S., Panak, P., Miteva, V., Boudakov, I., Bernhard, G. & Nitsche, H. ( 1999; ). Selective accumulation of heavy metals by three indigenous Bacillus strains, B. cereus, B. megaterium and B. sphaericus, from drain waters of a uranium waste pile. FEMS Microbiol Ecol 29, 59–67.[CrossRef]
    [Google Scholar]
  63. Selenska-Trajkowa, S., Radewa, G. & Markov, K. ( 1990; ). Comparison between Rhizobium galegae and Rhizobium meliloti plasmid contents. Lett Appl Microbiol 10, 123–126.[CrossRef]
    [Google Scholar]
  64. Sidhu, M. S. & Olsen, I. ( 1997; ). S-layer of Bacillus species. Microbiology 143, 1039–1052.[CrossRef]
    [Google Scholar]
  65. Stark, W. M., Boocock, M. R. & Sherratt, D. J. ( 1992; ). Catalysis by site-specific recombinases. Trends Genet 8, 432–439.[CrossRef]
    [Google Scholar]
  66. Takami, H., Han, C. G., Takaki, Y. & Ohtsubo, E. ( 2001; ). Identification and distribution of new insertion sequences in the genome of alkaliphilic Bacillus halodurans C-125. J Bacteriol 183, 4345–4356.[CrossRef]
    [Google Scholar]
  67. Thomas, S. R. & Trust, T. J. ( 1995; ). Tyrosine phosphorylation of the tetragonal paracrystalline array of Aeromonas hydrophila: molecular cloning and high-level expression of the S-layer gene. J Mol Biol 425, 568–581.
    [Google Scholar]
  68. Wintjens, R. & Rooman, M. ( 1996; ). Structural classification of HTH DNA-binding domains and protein-DNA interaction modes. J Mol Biol 262, 294–313.[CrossRef]
    [Google Scholar]
  69. Wood, H. E., Devine, K. M. & McConnell, D. J. ( 1990; ). Characterisation of a repressor gene (xre) and a temperature-sensitive allele from the Bacillus subtilis prophage, PBSX. Gene 96, 83–88.[CrossRef]
    [Google Scholar]
  70. Zuker, M., Mathews, D. H. & Turner, D. H. ( 1999; ). Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In RNA Biochemistry and Biotechnology (NATO ASI Series), pp. 11–43. Edited by J. Barciszewsk & B. F. C. Clark. Dordrecht: Kluwer.
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28201-0
Loading
/content/journal/micro/10.1099/mic.0.28201-0
Loading

Data & Media loading...

vol. , part 9, pp. 2961 - 2973

Oligonucleotides used for PCR and sequencing. [PDF file](16 kb)



PDF
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