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Functions of a hemolysin-like protein in the cyanobacterium Synechocystis sp. PCC 6803

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Abstract

A glucose-tolerant strain of the cyanobacterium Synechocystis sp. PCC 6803, generally referred to as wild type, produces a hemolysin-like protein (HLP) located on the cell surface. To analyze the function of HLP, we constructed a mutant in which the hlp gene was disrupted. The growth rate of the mutant was reduced when the cells were stressed by treatment with CuSO4, CdCl2, ZnCl2, ampicillin, kanamycin, or sorbitol in liquid medium, suggesting that HLP may increase cellular resistance to the inhibitory effects of these compounds. Uptake assays with 109Cd2+ using the silicone–oil layer centrifugation technique revealed that both wild type and mutant cells were labeled with 109Cd2+ within 1 min. Although the total radioactivity was much higher in the wild-type cells, 109Cd2+ incorporation was clearly much higher in the mutant cells after adsorbed 109Cd2+ was removed from the cell surface by washing with EDTA. These findings suggest that HLP functions as a barrier against the adsorption of toxic compounds.

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References

  • Baumann U, Wu S, Flaherty KM, McKay DB (1993) Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12:3357–3364

    PubMed  CAS  Google Scholar 

  • Brahamsha B (1996) An abundant cell-surface polypeptide is required for swimming by the nonflagellated marine cyanobacterium Synechococcus. Proc Natl Acad Sci USA 93:6504–6509

    Article  PubMed  CAS  Google Scholar 

  • Chojnacka K, Chojnacki A, Górecka H (2005) Biosorption of Cr3+, Cd2+ and Cu2+ ions by blue-green algae Spirulina sp.: kinetics, equilibrium and the mechanism of the process. Chemosphere 59:75–84

    Article  PubMed  CAS  Google Scholar 

  • De Philippis R, Sili C, Paperi R, Vincenzini M (2001) Exopolysaccharide-producing cyanobacteria and their possible exploitation: a review. J Appl Phycol 13:293–299

    Article  Google Scholar 

  • Decho AW (1990) Microbial exopolymer secretions in ocean environments–their role(s) in food webs and marine processes. Oceanogr Marine Biol Annu Rev 28:73–153

    Google Scholar 

  • Engelhardt H (2007) Are S-layers exoskeletons? The basic function of protein surface layers revisited. J Struct Biol 160:115–124

    Article  PubMed  CAS  Google Scholar 

  • Flemming HC (1993) Biofilms and environmental protection. Water Sci Technol 27:1–10

    CAS  Google Scholar 

  • Gilbert P, Das J, Foley I (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11:160–167

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Curtiss R 3rd (2009) Nickel-inducible lysis system in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 106:21550–21554

    Article  PubMed  CAS  Google Scholar 

  • Ludwig A (1996) Cytolytic toxins from gram-negative bacteria. Microbiologia 12:281–296

    PubMed  CAS  Google Scholar 

  • Mader C, Küpcü S, Sára M, Sleytr UB (1999) Stabilizing effect of an S-layer on liposomes towards thermal or mechanical stress. Biochim Biophys Acta 1418:106–116

    Article  PubMed  CAS  Google Scholar 

  • McCarren J, Heuser J, Roth R, Yamada N, Martone M, Brahamsha B (2005) Inactivation of swmA results in the loss of an outer cell layer in a swimming Synechococcus strain. J Bacteriol 187:224–230

    Article  PubMed  CAS  Google Scholar 

  • Merroun ML, 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

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot 57:235–247

    Article  PubMed  CAS  Google Scholar 

  • Obata T, Araie H, Shiraiwa Y (2004) Bioconcentration mechanism of selenium by a coccolithophorid, Emiliania huxleyi. Plant Cell Physiol 45:1434–1441

    Article  PubMed  CAS  Google Scholar 

  • Panoff JM, Priem B, Morvan H, Joset F (1988) Sulfated exopolysaccharides produced by two unicellular strains of cyanobacteria, Synechocystis PCC 6803 and PCC 6714. Arch Microbiol 150:558–563

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Sakiyama T, Ueno H, Homma H, Numata O, Kuwabara T (2006) Purification and characterization of a hemolysin-like protein, Sll1951, a nontoxic member of the RTX protein family from the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 188:3535–3542

    Article  PubMed  CAS  Google Scholar 

  • Sára M, Pum D, Sleytr UB (1992) Permeability and charge-dependent adsorption properties of the S-layer lattice from Bacillus coagulans E38–66. J Bacteriol 174:3487–3493

    PubMed  Google Scholar 

  • Schultze-Lam S, Harauz G, Beveridge TJ (1992) Participation of a cyanobacterial S-layer in fine-grain mineral formation. J Bacteriol 174:7971–7981

    PubMed  CAS  Google Scholar 

  • Silverstein A, Donatucci CF (2003) Bacterial biofilms and implantable prosthetic devices. Int J Impot Res 15:S150–S154

    Article  PubMed  Google Scholar 

  • Singh AK, Summerfield TC, Li H, Sherman LA (2006) The heat shock response in the cyanobacterium Synechocystis sp. strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch Microbiol 186:273–286

    Article  PubMed  CAS  Google Scholar 

  • Sleytr UB, Messner P (2000) Crystalline bacterial cell surface layers. In: Lederberg J (ed) Encyclopedia of microbiology, 2nd edn. Academic Press, San Diego, pp 899–906

    Google Scholar 

  • Šmarda J, Šmajs D, Komrska J, Krzyžánek V (2002) S-layers on cell walls of cyanobacteria. Micron 33:257–277

    Article  PubMed  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Tang JL et al (2009) Detection of metal binding sites on functional S-layer nanoarrays using single molecule force spectroscopy. J Struct Biol 168:217–222

    Article  PubMed  CAS  Google Scholar 

  • Vaara T (1982) The outermost surface-structures in Chroococcacean cyanobacteria. Can J Microbiol 28:929–941

    Article  Google Scholar 

  • Wiles TJ, Kulesus RR, Mulvey MA (2008) Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85:11–19

    Article  PubMed  CAS  Google Scholar 

  • Williams JGK (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic-engineering methods in Synechocystis 6803. Methods Enzymol 167:766–778

    Article  CAS  Google Scholar 

  • Yubuki N, Inagaki Y, Nakayama T, Inouye I (2007) Ultrastructure and ribosomal RNA phylogeny of the free-living heterotrophic flagellate Dysnectes brevis n. gen., n. sp., a new member of the Fornicata. J Eukaryot Microbiol 54:191–200

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. T. Kuwabara for his critical discussion and advice, and Dr. T. Hama and Miss M. Sawai for operation of the flow cytometer, all of whom are at the University of Tsukuba (UT). The radiolabeling experiments were performed in the Radioisotope Center of UT with their kind help, especially in the 109Cd uptake experiments.

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Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, 305-8572, Japan

    Tetsushi Sakiyama, Hiroya Araie, Iwane Suzuki & Yoshihiro Shiraiwa

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  1. Tetsushi Sakiyama
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  2. Hiroya Araie
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  3. Iwane Suzuki
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  4. Yoshihiro Shiraiwa
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Corresponding author

Correspondence to Yoshihiro Shiraiwa.

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Communicated by ErkoStackebrandt.

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Sakiyama, T., Araie, H., Suzuki, I. et al. Functions of a hemolysin-like protein in the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 193, 565–571 (2011). https://doi.org/10.1007/s00203-011-0700-2

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  • DOI: https://doi.org/10.1007/s00203-011-0700-2

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