1887

Abstract

JG-B53 was isolated from the uranium mining waste pile Haberland near Johanngeorgenstadt, Germany. Previous studies have shown that many bacteria that have been isolated from these heavy metal contaminated environments possess surface layer (S-layer) proteins that enable the bacteria to survive by binding metals with high affinity. Conversely, essential trace elements are able to cross the filter layer and reach the interior of the cell. This is especially true of the S-layer of JG-B53, which possesses outstanding recrystallization and metal-binding properties. In this study, S-layer protein gene sequences encoded in the genome of JG-B53 were identified using next-generation sequencing technology followed by bioinformatic analyses. The genome of JG-B53 encodes at least eight putative S-layer protein genes with distinct differences. Using mRNA analysis the expression of the putative S-layer protein genes was studied. The functional S-layer protein B53 Slp1 was identified as the dominantly expressed S-layer protein in JG-B53 by mRNA studies, SDS-PAGE and N-terminal sequencing. B53 Slp1 is characterized by square lattice symmetry and a molecular mass of 116 kDa. The S-layer protein B53 Slp1 shows a high similarity to the functional S-layer protein of JG-A12, which was isolated from the same uranium mining waste pile Haberland and has been described by previous research. These similarities indicate horizontal gene transfer and DNA rearrangements between these bacteria. The presence of multiple S-layer gene copies may enable the bacterial strains to quickly adapt to changing environments.

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2013-06-01
2019-12-05
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References

  1. Bahl H. , Scholz H. , Bayan N. . & other authors ( 1997; ). Molecular biology of S-layers. . FEMS Microbiol Rev 20:, 47–98. [CrossRef]
    [Google Scholar]
  2. Bendtsen J. D. , Nielsen H. , von Heijne G. , Brunak S. . ( 2004; ). Improved prediction of signal peptides: SignalP 3.0. . J Mol Biol 340:, 783–795. [CrossRef]
    [Google Scholar]
  3. 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]
  4. Boot H. J. , Kolen C. P. , Pouwels P. H. . ( 1996; ). 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]
  5. Borst P. , Greaves D. R. . ( 1987; ). Programmed gene rearrangements altering gene expression. . Science 235:, 658–667. [CrossRef]
    [Google Scholar]
  6. Claus H. , Akca E. , Debaerdemaeker T. , Evrard C. , Declercq J. P. , König H. . ( 2002; ). Primary structure of selected archaeal mesophilic and extremely thermophilic outer surface layer proteins. . Syst Appl Microbiol 25:, 3–12. [CrossRef]
    [Google Scholar]
  7. Claus H. , Akca E. , Debaerdemaeker T. , Evrard C. , Declercq J. P. , Harris J. R. , Schlott B. , König H. . ( 2005; ). Molecular organization of selected prokaryotic S-layer proteins. . Can J Microbiol 51:, 731–743. [CrossRef]
    [Google Scholar]
  8. Dohm N. , Petri A. , Schlander M. , Schlott B. , König H. , Claus H. . ( 2011; ). Molecular and biochemical properties of the S-layer protein from the wine bacterium Lactobacillus hilgardii B706. . Arch Microbiol 193:, 251–261. [CrossRef]
    [Google Scholar]
  9. 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]
  10. Engelhardt H. , Saxton W. O. , Baumeister W. . ( 1986; ). Three-dimensional structure of the tetragonal surface layer of Sporosarcina ureae. . J Bacteriol 168:, 309–317.
    [Google Scholar]
  11. Fahmy K. , Merroun M. , Pollmann K. , Raff J. , Savchuk O. , Hennig C. , Selenska-Pobell S. . ( 2006; ). Secondary structure and Pd(II) coordination in S-layer proteins from Bacillus sphaericus studied by infrared and X-ray absorption spectroscopy. . Biophys J 91:, 996–1007. [CrossRef]
    [Google Scholar]
  12. Fernández L. A. , Berenguer J. . ( 2000; ). Secretion and assembly of regular surface structures in Gram-negative bacteria. . FEMS Microbiol Rev 24:, 21–44.[CrossRef]
    [Google Scholar]
  13. He M. Y. , Li X. Y. , Liu H. L. , Miller S. J. , Wang G. J. , Rensing C. . ( 2011; ). Characterization and genomic analysis of a highly chromate resistant and reducing bacterial strain Lysinibacillus fusiformis ZC1. . J Hazard Mater 185:, 682–688. [CrossRef]
    [Google Scholar]
  14. Hiemenz P. C. , Rajagopalan R. . ( 1977; ). Principles of colloid and surface chemistry. New York:: CRC Press;.
    [Google Scholar]
  15. Houwink A. L. . ( 1953; ). A macromolecular mono-layer in the cell wall of Spirillum spec. . Biochim Biophys Acta 10:, 360–366. [CrossRef]
    [Google Scholar]
  16. Huang X. Q. , Miller W. . ( 1991; ). A time-efficient, linear-space local similarity algorithm. . Adv Appl Math 12:, 337–357. [CrossRef]
    [Google Scholar]
  17. 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]
  18. Jakava-Viljanen M. , Avall-Jääskeläinen 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]
  19. Jroundi F. , Merroun M. L. , Arias J. M. , Rossberg A. , Selenska-Pobell S. , González-Munoz M. T. . ( 2007; ). Spectroscopic and microscopic characterization of uranium biomineralization in Myxococcus xanthus. . Geomicrobiol J 24:, 441–449. [CrossRef]
    [Google Scholar]
  20. Kawai E. , Akatsuka H. , Idei A. , Shibatani T. , Omori K. . ( 1998; ). Serratia marcescens S-layer protein is secreted extracellularly via an ATP-binding cassette exporter, the Lip system. . Mol Microbiol 27:, 941–952. [CrossRef]
    [Google Scholar]
  21. Kern W. , Puotinen D. A. . ( 1970; ). Cleaning solutions based on hydrogen peroxide for use in silicon semiconductor technology. . RCA Review 31:, 187–206.
    [Google Scholar]
  22. 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]
  23. 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]
  24. Lemaire M. , Ohayon H. , Gounon P. , Fujino T. , Béguin P. . ( 1995; ). OlpB, a new outer layer protein of Clostridium thermocellum, and binding of its S-layer-like domains to components of the cell envelope. . J Bacteriol 177:, 2451–2459.
    [Google Scholar]
  25. Lupas A. , Engelhardt H. , Peters J. , Santarius U. , Volker S. , Baumeister W. . ( 1994; ). Domain structure of the Acetogenium kivui surface layer revealed by electron crystallography and sequence analysis. . J Bacteriol 176:, 1224–1233.
    [Google Scholar]
  26. Martinez R. J. , Wang Y. , Raimondo M. A. , Coombs J. M. , Barkay T. , Sobecky P. A. . ( 2006; ). Horizontal gene transfer of PIB-type ATPases among bacteria isolated from radionuclide- and metal-contaminated subsurface soils. . Appl Environ Microbiol 72:, 3111–3118. [CrossRef]
    [Google Scholar]
  27. Merroun M. , Pollmann K. , Raff J. , Scheinost A. , Selenska-Pobell S. . ( 2003; ). EXAFS studies of palladium nanoclusters formed at the cells and S-layers of Bacillus sphaericus JG-A12. . FZR-Report no. Forschungszentrum Dresden-Rossendorf Rep 400:, 25.
    [Google Scholar]
  28. Merroun M. L. , Raff J. , Rossberg A. , Hennig C. , Reich T. , Selenska-Pobell S. . ( 2005; ). Complexation of uranium by cells and S-layer sheets of Bacillus sphaericus JG-A12. . Appl Environ Microbiol 71:, 5532–5543. [CrossRef]
    [Google Scholar]
  29. Messner P. , Sleytr U. B. . ( 1991; ). Bacterial surface layer glycoproteins. . Glycobiology 1:, 545–551. [CrossRef]
    [Google Scholar]
  30. 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]
  31. 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]
  32. Nakamura Y. , Itoh T. , Matsuda H. , Gojobori T. . ( 2004; ). Biased biological functions of horizontally transferred genes in prokaryotic genomes. . Nat Genet 36:, 760–766. [CrossRef]
    [Google Scholar]
  33. Nedelkova M. , Merroun M. L. , Rossberg A. , Hennig C. , Selenska-Pobell S. . ( 2007; ). Microbacterium isolates from the vicinity of a radioactive waste depository and their interactions with uranium. . FEMS Microbiol Ecol 59:, 694–705. [CrossRef]
    [Google Scholar]
  34. Petersen T. N. , Brunak S. , von Heijne G. , Nielsen H. . ( 2011; ). SignalP 4.0: discriminating signal peptides from transmembrane regions. . Nat Methods 8:, 785–786. [CrossRef]
    [Google Scholar]
  35. Pink T. , Langer K. , Hotzy C. , Sára M. . ( 1996; ). Regulation of S-layer protein synthesis of Bacillus stearothermophilus PV72 through variation of continuous cultivation conditions. . J Biotechnol 50:, 189–200. [CrossRef]
    [Google Scholar]
  36. Pollmann K. , Raff J. , Schnorpfeil M. , Radeva G. , Selenska-Pobell S. . ( 2005; ). Novel surface layer protein genes in Bacillus sphaericus associated with unusual insertion elements. . Microbiology 151:, 2961–2973. [CrossRef]
    [Google Scholar]
  37. Pollmann K. , Raff J. , Merroun M. , Fahmy K. , Selenska-Pobell S. . ( 2006; ). Metal binding by bacteria from uranium mining waste piles and its technological applications. . Biotechnol Adv 24:, 58–68. [CrossRef]
    [Google Scholar]
  38. Pum D. , Sleytr U. B. . ( 1994; ). Large-scale reconstitution of crystalline bacterial surface-layer proteins at the air–water-interface and on lipid films. . Thin Solid Films 244:, 882–886. [CrossRef]
    [Google Scholar]
  39. Pum D. , Weinhandl M. , Hödl C. , Sleytr U. B. . ( 1993; ). Large-scale recrystallization of the S-layer of Bacillus coagulans E38–66 at the air/water interface and on lipid films. . J Bacteriol 175:, 2762–2766.
    [Google Scholar]
  40. Raff J. . ( 2002; ). Wechselwirkungen der Hüllproteine von Bakterien aus Uranabfallhalden mit Schwermetallen . . PhD thesis, University of Leipzig:. FZR-Report no. 358. Forschungszentrum Dresden-Rossendorf Rep.
  41. 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:, 24.
    [Google Scholar]
  42. Renart J. , Reiser J. , Stark G. R. . ( 1979; ). Transfer of proteins from gels to diazobenzyloxymethyl-paper and detection with antisera: a method for studying antibody specificity and antigen structure. . Proc Natl Acad Sci U S A 76:, 3116–3120. [CrossRef]
    [Google Scholar]
  43. Sambrook J. , Fritsch E. F. , Maniatis T. . ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn . Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  44. Sára M. , Sleytr U. B. . ( 1987; ). Molecular sieving through S layers of Bacillus stearothermophilus strains. . J Bacteriol 169:, 4092–4098.
    [Google Scholar]
  45. Sára M. , Sleytr U. B. . ( 2000; ). S-layer proteins. . J Bacteriol 182:, 859–868. [CrossRef]
    [Google Scholar]
  46. Sára M. , Kuen B. , Mayer H. F. , Mandl F. , Schuster K. C. , Sleytr U. B. . ( 1996; ). Dynamics in oxygen-induced changes in S-layer protein synthesis from Bacillus stearothermophilus PV72 and the S-layer-deficient variant T5 in continuous culture and studies of the cell wall composition. . J Bacteriol 178:, 2108–2117.
    [Google Scholar]
  47. Sára M. , Pum D. , Schuster B. , Sleytr U. B. . ( 2005; ). S-layers as patterning elements for application in nanobiotechnology. . J Nanosci Nanotechnol 5:, 1939–1953. [CrossRef]
    [Google Scholar]
  48. Schäffer C. , Graninger M. , Messner P. . ( 2001; ). Prokaryotic glycosylation. . Proteomics 1:, 248–261. [CrossRef]
    [Google Scholar]
  49. 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]
  50. Schurtenberger P. , Newman M. E. . ( 1993; ). Characterization of Biological and Environmental Particles Using Static and Dynamic Light Scattering. Boca Raton, FL:: Lewis Publishers;.
    [Google Scholar]
  51. 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]
  52. Sleytr U. B. , Beveridge T. J. . ( 1999; ). Bacterial S-layers. . Trends Microbiol 7:, 253–260. [CrossRef]
    [Google Scholar]
  53. Sleytr U. B. , Messner P. . ( 1988; ). Crystalline surface layers in procaryotes. . J Bacteriol 170:, 2891–2897.
    [Google Scholar]
  54. Sleytr U. B. , Sára M. . ( 1997; ). Bacterial and archaeal S-layer proteins: structure-function relationships and their biotechnological applications. . Trends Biotechnol 15:, 20–26. [CrossRef]
    [Google Scholar]
  55. Sleytr U. B. , Messner P. , Pum D. , Sára M. . ( 1999; ). Crystalline bacterial cell surface layers (S layers): from supramolecular cell structure to biomimetics and nanotechnology. . Angew Chem Int Edn 38:, 1034–1054. [CrossRef]
    [Google Scholar]
  56. Smith S. H. , Murray R. G. . ( 1990; ). The structure and associations of the double S layer on the cell wall of Aquaspirillum sinuosum. . Can J Microbiol 36:, 327–335. [CrossRef]
    [Google Scholar]
  57. Solovyev V. V. , Shahmuradov I. A. . ( 2003; ). PromH: promoters identification using orthologous genomic sequences. . Nucleic Acids Res 31:, 3540–3545. [CrossRef]
    [Google Scholar]
  58. Sprott G. D. , Koval S. F. , Schnaitman C. A. . ( 1994; ). In Methods for General and Molecular Bacteriology: Cell Fractionation, pp. 72–103. Edited by P. Gerhardt, R. G. E. Murray, W. A. Wood & N. R. Krieg . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  59. Towbin H. , Staehelin T. , Gordon J. . ( 1979; ). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. . Proc Natl Acad Sci U S A 76:, 4350–4354. [CrossRef]
    [Google Scholar]
  60. Tsuboi A. , Tsukagoshi N. , Udaka S. . ( 1982; ). Reassembly in vitro of hexagonal surface arrays in a protein-producing bacterium, Bacillus brevis 47. . J Bacteriol 151:, 1485–1497.
    [Google Scholar]
  61. Walker J. M. . ( 2009; ). SDS polyacrylamide gel electrophoresis of proteins. . In The Protein Protocols Handbook, pp. 177–185. Edited by Walker J. M. . . Springer: Humana Press;.
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