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Rotating wall vessel exposure alters protein secretion and global gene expression in Staphylococcus aureus

Published online by Cambridge University Press:  05 December 2011

Helena Rosado ,
Alex J. O'Neill ,
Katy L. Blake ,
Meik Walther ,
Paul F. Long ,
Jason Hinds  and
Peter W. Taylor
Helena Rosado
Affiliation:
School of Pharmacy, University College London, 29-39 Brunswick Square, London WC1N 1AC, UK
Alex J. O'Neill
Affiliation:
Institute of Molecular and Cellular Biology, University of Leeds, Leeds LS2 9JT, UK
Katy L. Blake
Affiliation:
Institute of Molecular and Cellular Biology, University of Leeds, Leeds LS2 9JT, UK
Meik Walther
Affiliation:
Abteilung Genetik, Technische Universität Kaiserslautern, Postfach 3049, Paul-Ehrlich-Straβe 24, 67653 Kaiserslautern, Germany
Paul F. Long
Affiliation:
Institute of Pharmaceutical Science, King's College, Franklin-Wilkins Building, 150 Stamford Street, London SE1 9NH, UK
Jason Hinds
Affiliation:
Department of Cellular and Molecular Medicine, St. George's, University of London, Cranmer Terrace, Tooting London SW17 0RE, UK
Peter W. Taylor*
Affiliation:
School of Pharmacy, University College London, 29-39 Brunswick Square, London WC1N 1AC, UK
*
e-mail: peter.taylor@pharmacy.ac.uk
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Abstract

Staphylococcus aureus is routinely recovered from air and surface samples taken aboard the International Space Station (ISS) and poses a health threat to crew. As bacteria respond to the low shear forces engendered by continuous rotation conditions in a Rotating Wall Vessel (RWV) and the reduced gravitational field of near-Earth flight by altering gene expression, we examined the effect of low-shear RWV growth on protein secretion and gene expression by three S. aureus isolates. When cultured under 1 g, the total amount of protein secreted by these strains varied up to fourfold; under continuous rotation conditions, protein secretion by all three strains was significantly reduced. Concentrations of individual proteins were differentially reduced and no evidence was found for increased lysis. These data suggest that growth under continuous rotation conditions reduces synthesis or secretion of proteins. A limited number of changes in gene expression under continuous rotation conditions were noted: in all isolates vraX, a gene encoding a polypeptide associated with cell wall stress, was down-regulated. A vraX deletion mutant of S. aureus SH1000 was constructed: no differences were found between SH1000 and ΔvraX with respect to colony phenotype, viability, protein export, antibiotic susceptibility, vancomycin kill kinetics, susceptibility to cold or heat and gene modulation. An ab initio protein–ligand docking simulation suggests a major binding site for β-lactam drugs such as imipenem. If such changes to the bacterial phenotype occur during spaceflight, they will compromise the capacity of staphylococci to cause systemic infection and to circumvent antibacterial chemotherapy.

Keywords

bacterial microarraycontinuous rotation conditionsexoproteomeStaphylococcus aureusvraX
Type
Research Article
Information
International Journal of Astrobiology , Volume 11 , Issue 2 , April 2012 , pp. 71 - 81
Copyright
Copyright © Cambridge University Press 2011

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References

Bae, T. & Schneewind, O. (2006). Plasmid 55, 58–63.CrossRefGoogle Scholar
Benoit, M. & Klaus, D.M. (2007). Adv. Space Res. 39, 1225–1232.CrossRefGoogle Scholar
Bernal, P., Lemaire, S., Pinho, M.G., Mobashery, S., Hinds, J. & Taylor, P.W. (2010). J. Biol. Chem. 285, 24 055–24 065.CrossRefGoogle Scholar
Boël, G., Pichereau, V., Mijakovic, I., Mazé, A., Poncet, S., Gillet, S., Giard, J.-C., Hartke, A., Auffray, Y. & Deutscher, J. (2004). J. Mol. Biol. 337, 485–496.CrossRefGoogle Scholar
Damblon, C., Raquet, X., Lian, L.Y., Lamotte-Brasseur, J., Fonze, E., Charlier, P., Roberts, G.C. & Frère, J.M. (1996). Proc. Natl. Acad. Sci. USA 93, 1747–1752.CrossRefGoogle Scholar
Du, B., Daniels, V.R., Vaksman, Z., Boyd, J.L., Crady, C. & Putcha, L. (2011). AAPS J. 13, 299–308.CrossRefGoogle Scholar
Giraudo, A.T., Cheung, A.L. & Nagel, R. (1997). Arch. Microbiol. 168, 53–58.CrossRefGoogle Scholar
Hammond, T.G. & Hammond, J.M. (2001). Am. J. Physiol. Renal Physiol. 281, 12–25.CrossRefGoogle Scholar
Horsburgh, M.J., Aish, J.L., White, I.J., Shaw, L., Lithgow, J.K. & Foster, S.J. (2002). J. Bacteriol. 184, 5457–5467.CrossRefGoogle Scholar
Jones, R.C., Deck, J., Edmondson, R.D. & Hart, M.E. (2008). J. Bacteriol. 190, 5265–5278.CrossRefGoogle Scholar
Juergensmeyer, M.A., Juergensmeyer, E.A. & Guikema, J.A. (1999). Micrograv. Sci. Technol. 12, 41–47.Google Scholar
Klaus, D.M. (2002). In Encyclopedia of Environmental Microbiology, ed. Britton, G., pp. 2996–3004. John Wiley and Sons, New York.Google Scholar
Lapchine, L., Moatti, N., Gasset, G., Richoilley, G., Templier, J. & Tixador, R. (1985). Drugs Exp. Clin. Res. 12, 933–938.Google Scholar
Leaver-Fay, A., Tyka, M., Lewis, S.M., Lange, O.F., Thompson, J., Jacak, R., Kaufman, K., Renfrew, P.D., Smith, C.A., Sheffler, W. et al. (2011). Methods Enzymol. 487, 545–574.CrossRefGoogle Scholar
Lui, G.Y., Essex, A., Buchanan, J.T., Datta, V., Hoffman, H.M., Bastian, J.F., Fierer, J. & Nizet, V. (2005). J. Exp. Med. 202, 209–215.Google Scholar
McAleese, F., Wu, S.W., Sieradzki, K., Dunman, P., Murphy, E., Projan, S. & Tomasz, A. (2006). J. Bacteriol. 188, 1120–1133.CrossRefGoogle Scholar
Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S. & Olson, A.J. (2009). J. Comput. Chem. 30, 2785–2791.CrossRefGoogle Scholar
Muthaiyan, A., Silverman, J.A., Jayaswal, R.K. & Wilkinson, B.J. (2008). Antimicrob. Agents Chemother. 52, 980–990.CrossRefGoogle Scholar
Nauman, E.A., Ott, C.M., Sander, E., Tucker, D.L., Pierson, D., Wilson, J.W. & Nickerson, C.A. (2007). Appl. Environ. Microbiol. 73, 699–705.CrossRefGoogle Scholar
Nickerson, C.A., Ott, C.M., Mister, S.J., Morrow, B.J., Burns-Keliher, L. & Pierson, D.L., (2000). Infect. Immun. 68, 3147–3152.CrossRefGoogle Scholar
Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R., LeBlanc, L., Höner zu Bentrup, K., Hammond, T. & Pierson, D.L. (2000). J. Microbiol. Meth. 54, 1–11.CrossRefGoogle Scholar
Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R. & Pierson, D.L. (2004). Microbiol. Mol. Biol. Rev. 68, 345–361.CrossRefGoogle Scholar
Novick, R.P. (2003). Mol. Microbiol. 48, 1429–1449.CrossRefGoogle Scholar
Novick, R.P. & Jiang, D. (2003). Microbiology 149, 2709–2717.CrossRefGoogle Scholar
Novikova, N. (2004). Microbiol. Ecol. 47, 127–132.CrossRefGoogle Scholar
Novikova, N., De Boever, P., Poddubko, S., Deshevaya, E., Polikarpov, N., Rakova, N., Coninx, I. & Mergeay, M. (2006). Res. Microbiol. 157, 5–12.CrossRefGoogle Scholar
O'Neill, A.J. (2010). Lett. Appl. Microbiol. 51, 358–361.CrossRefGoogle Scholar
Rohl, C.A., Strauss, C.E., Misura, K.M. & Baker, D. (2004). Methods Enzymol. 383, 66–93.CrossRefGoogle Scholar
Rosado, H., Doyle, M., Hinds, J. & Taylor, P.W. (2010). Acta Astronaut. 66, 408–413.CrossRefGoogle Scholar
Scherl, A., François, P., Charbonnier, Y., Deshusses, J.M., Koessler, T., Huyghe, A., Bento, M., Stahl-Zeng, J., Fischer, A., Masselot, A. et al. (2006). BMC Genom. 7, 296.CrossRefGoogle Scholar
Schwartz, R.P., Goodwin, T.J. & Wolf, D.A. (1992). J. Tiss. Cult. Meth. 14, 51–58.CrossRefGoogle Scholar
Sibbald, M.J.J.B., Ziebandt, A.K., Engelmann, S., Hecker, M., de Jong, A., Harmsen, H.J.M., Raangs, G.C., Stokroos, I., Arends, J.P., Dubois, J.Y.F. et al. (2006). Microbiol. Mol. Biol. Rev. 70, 755–788.CrossRefGoogle Scholar
Sonnenfeld, G. (2005). Curr. Pharm. Biotechnol. 6, 343–349.CrossRefGoogle Scholar
Sonnenfeld, G. & Shearer, W.T. (2002). Nutrition 18, 899–903.CrossRefGoogle Scholar
Stapleton, M.R., Horsburgh, M.J., Hayhurst, E.J., Wright, L., Jonsson, I.-M., Tarkowski, A., Kokai-Kun, J.F., Mond, J.J. & Foster, S.J. (2007). J. Bacteriol. 189, 7316–7325.CrossRefGoogle Scholar
Taylor, G.R. (1974). Aerospace Med. 45, 824–882.Google Scholar
Taylor, P.W. & Rosado, H. (2007). Planet Mars Research Focus, ed. Costas, L.A., pp. 165–185. Nova Science, Hauppauge, NY.Google Scholar
Tixador, R., Richoilley, G., Gasset, G., Templier, J., Bes, J.C., M`oatti, N. & Lapchine, L. (1985). Aviat. Space Environ. Med. 56, 748–751.Google Scholar
Tjalsma, H., Anteman, H., Jongbloed, J.D.H., Braun, P.G., Darmon, E., Dorenbos, R., Dubois, J.-Y.F., Westers, H., Zanen, G., Quax, W.J. et al. (2004). Microbiol. Mol. Biol. Rev. 68, 207–233.CrossRefGoogle Scholar
Utaida, S., Dunman, P.M., Macapagal, D., Murphy, E., Projan, S.J., Singh, V.K., Jayaswal, R.K. & Wilkinson, B.J. (2003). Microbiology 149, 2719–2732.CrossRefGoogle Scholar
Wilson, J.W., Ramamurthy, R., Porwollick, S., McClelland, M., Hammond, T., Allen, P., Ott, C.M., Pierson, D.L. & Nickerson, C.A. (2002). Proc. Natl. Acad. Sci. U.S.A. 99, 13 807–13 812.CrossRefGoogle Scholar
Wilson, J.W., Ott, C.M., Höner zu Bentrup, K., Ramamurthy, R., Quick, L., Porwollik, S., Cheng, P., McClelland, M., Tsaprailis, G., Radabaugh, T. et al. (2007). Proc. Natl. Acad. Sci. U.S.A. 104, 16299–16 304.CrossRefGoogle Scholar
Wilson, J.W., Ott, C.M., Quick, L., Davis, R., Höner zu Bentrup, K., Crabbé, A., Richter, E., Sarker, S., Barrila, J., Porwollik, S. et al. (2008). PLoS ONE 3, e3923.CrossRefGoogle Scholar
Witney, A.A., Marsden, G.L., Holden, M.T., Stabler, R.A., Husain, S.E., Vass, J.K., Butcher, P.D., Hinds, J. & Lindsay, J.A. (2005). Appl. Environ. Microbiol. 71, 7504–7514.CrossRefGoogle Scholar
Ziebandt, A.K., Becher, D., Ohlsen, K., Hacker, J., Hecker, M. & Engelmann, S. (2004). Proteomics 4, 3034–3047.Google Scholar
Ziebandt, A.K., Weber, H., Rudolph, J., Schmid, R., Hoper, D., Engelmann, S. & Hecker, M. (2001). Proteomics 1, 480–493.3.0.CO;2-O>CrossRefGoogle Scholar