Transcriptomic Responses of Germinating Bacillus subtilis Spores Exposed to 1.5 Years of Space and Simulated Martian Conditions on the EXPOSE-E Experiment PROTECT
Abstract
Because of their ubiquity and resistance to spacecraft decontamination, bacterial spores are considered likely potential forward contaminants on robotic missions to Mars. Thus, it is important to understand their global responses to long-term exposure to space or martian environments. As part of the PROTECT experiment, spores of B. subtilis 168 were exposed to real space conditions and to simulated martian conditions for 559 days in low-Earth orbit mounted on the EXPOSE-E exposure platform outside the European Columbus module on the International Space Station. Upon return, spores were germinated, total RNA extracted, fluorescently labeled, and used to probe a custom Bacillus subtilis microarray to identify genes preferentially activated or repressed relative to ground control spores. Increased transcript levels were detected for a number of stress-related regulons responding to DNA damage (SOS response, SPβ prophage induction), protein damage (CtsR/Clp system), oxidative stress (PerR regulon), and cell envelope stress (SigV regulon). Spores exposed to space demonstrated a much broader and more severe stress response than spores exposed to simulated martian conditions. The results are discussed in the context of planetary protection for a hypothetical journey of potential forward contaminant spores from Earth to Mars and their subsequent residence on Mars. Key Words: Bacillus—Mars—Planetary protection—Spaceflight—Spores. Astrobiology 12, 469–486.
Get full access to this article
View all available purchase options and get full access to this article.
Abbreviations
ANOVA, analysis of variance; COSPAR, the Committee on Space Research; ds, double strand; ECF, extracytoplasmic function; ISS, International Space Station; LB, Luria-Bertani; ORF, open reading frame; PBS, phosphate-buffered saline; SASP, small, acid-soluble spore protein; UF-ICBR, University of Florida Interdisciplinary Center for Biotechnology Research.
References
Au N.Kuester-Schoeck E.Mandava V.Bothwell L.E.Canny S.P.Chachu K.Colavito S.A.Fuller S.N.Groban E.S.Hensley L.A.O'Brien T.C.Shah A.Tierney J.T.Tomm L.L.O'Gara T.M.Goranov A.I.Grossman A.D.Lovett C.M.2005. Genetic composition of the Bacillus subtilis SOS systemJ Bacteriol1877655-7666. Au, N., Kuester-Schoeck, E., Mandava, V., Bothwell, L.E., Canny, S.P., Chachu, K., Colavito, S.A., Fuller, S.N., Groban, E.S., Hensley, L.A., O'Brien, T.C., Shah, A., Tierney, J.T., Tomm, L.L., O'Gara, T.M., Goranov, A.I., Grossman, A.D., and Lovett, C.M. (2005) Genetic composition of the Bacillus subtilis SOS system. J Bacteriol 187:7655–7666.
Berlett B.S.Stadtman E.R.1997. Protein oxidation in aging, disease, and oxidative stressJ Biol Chem27220313-20316. Berlett, B.S. and Stadtman, E.R. (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272:20313–20316.
Bruckner J.Venkateswaran K.Osman S.Conley C.2009. Space microbiology: planetary protection, burden, diversity and significance of spacecraft associated microbesEncyclopedia of Microbiology3rdElsevierOxford52-65. Bruckner, J., Venkateswaran, K., Osman, S., and Conley, C. (2009) Space microbiology: planetary protection, burden, diversity and significance of spacecraft associated microbes. In Encyclopedia of Microbiology, 3rd ed., Elsevier, Oxford, pp 52–65.
Carrasco B.Cozar M.C.Lurz R.Alonso J.C.Ayora S.2004. Genetic recombination in Bacillus subtilis 168: contribution of Holliday junction processing functions in chromosome segregationJ Bacteriol1865557-5566. Carrasco, B., Cozar, M.C., Lurz, R., Alonso, J.C., and Ayora, S. (2004) Genetic recombination in Bacillus subtilis 168: contribution of Holliday junction processing functions in chromosome segregation. J Bacteriol 186:5557–5566.
Chaturongakul S.Raengpradub S.Palmer M.E.Bergholz T.M.Orsi R.H.Hu Y.Ollinger J.Wiedmann M.Boor K.J.2011. Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors σB, σC, σH, and σL in Listeria monocytogenesAppl Environ Microbiol77187-200. Chaturongakul, S., Raengpradub, S., Palmer, M.E., Bergholz, T.M., Orsi, R.H., Hu, Y., Ollinger, J., Wiedmann, M., and Boor, K.J. (2011) Transcriptomic and phenotypic analyses identify coregulated, overlapping regulons among PrfA, CtsR, HrcA, and the alternative sigma factors σB, σC, σH, and σL in Listeria monocytogenes. Appl Environ Microbiol 77:187–200.
COSPAR2011COSPAR Planetary Protection Policy (2002, amended 2011)COSPARParishttp://cosparhq.cnes.fr/Scistr/PPPolicy%20(24Mar2011).pdf. COSPAR. (2011) COSPAR Planetary Protection Policy (2002, amended 2011), COSPAR, Paris. Available online at http://cosparhq.cnes.fr/Scistr/PPPolicy%20(24Mar2011).pdf.
Driks A.1999. Bacillus subtilis spore coatMicrobiol Mol Biol Rev631-20. Driks, A. (1999) Bacillus subtilis spore coat. Microbiol Mol Biol Rev 63:1–20.
Elsholz A.K.W.Michalik S.Zuehlke D.Hecker M.Gerth U.2010. CtsR, the Gram-positive master regulator of protein quality control, feels the heatEMBO J293621-3629. Elsholz, A.K.W., Michalik, S., Zuehlke, D., Hecker, M., and Gerth, U. (2010) CtsR, the Gram-positive master regulator of protein quality control, feels the heat. EMBO J 29:3621–3629.
Fajardo-Cavazos P.Schuerger A.C.Nicholson W.L2007. Testing interplanetary transfer of bacteria by natural impact phenomena and human spaceflight activitiesActa Astronaut60534-540. Fajardo-Cavazos, P., Schuerger, A.C., and Nicholson W.L. (2007) Testing interplanetary transfer of bacteria by natural impact phenomena and human spaceflight activities. Acta Astronaut 60:534–540.
Fajardo-Cavazos P.Schuerger A.C.Nicholson W.L.2010. Exposure of DNA and Bacillus subtilis spores to simulated Mars environment: use of quantitative PCR (qPCR) to measure inactivation rates of DNA to function as a template moleculeAstrobiology10403-411. Fajardo-Cavazos, P., Schuerger, A.C., and Nicholson, W.L. (2010) Exposure of DNA and Bacillus subtilis spores to simulated Mars environment: use of quantitative PCR (qPCR) to measure inactivation rates of DNA to function as a template molecule. Astrobiology 10:403–411.
Faulkner M.J.Helmann J.D.2011. Peroxide stress elicits adaptive changes in bacterial metal homeostasisAntioxid Redox Signal15175-189. Faulkner, M.J. and Helmann, J.D. (2011) Peroxide stress elicits adaptive changes in bacterial metal homeostasis. Antioxid Redox Signal 15:175–189.
Friedberg E.C.Walker G.C.Siede W.Wood R.D.Schultz R.A.Ellenberger T.2006DNA Repair and Mutagenesis2ndASM PressWashington DC. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, R.A., and Ellenberger, T. (2006) DNA Repair and Mutagenesis, 2nd ed., ASM Press, Washington DC.
Gerhardt P.Murray R.G.E.Costilow R.N.Nester E.W.Wood W.A.Krieg N.R.Phillips G.B.1981Manual of Methods for General BacteriologyASM PressWashington DC. Gerhardt, P., Murray, R.G.E., Costilow, R.N., Nester, E.W., Wood, W.A., Krieg, N.R., and Phillips, G.B., editors. (1981) Manual of Methods for General Bacteriology, ASM Press, Washington DC.
Gerth U.Kirstein J.Mostertz J.Waldminghaus T.Miethke M.Kock H.Hecker M.2004. Fine-tuning in regulation of Clp protein content in Bacillus subtilisJ Bacteriol186179-191. Gerth, U., Kirstein, J., Mostertz, J., Waldminghaus, T., Miethke, M., Kock, H., and Hecker, M. (2004) Fine-tuning in regulation of Clp protein content in Bacillus subtilis. J Bacteriol 186:179–191.
Goranov A.I.Kuester-Schoeck E.Wang J.D.Grossman A.D.2006. Characterization of the global transcriptional responses of different types of DNA damage and disruption of replication in Bacillus subtilisJ Bacteriol1885595-5605. Goranov, A.I., Kuester-Schoeck, E., Wang, J.D., and Grossman, A.D. (2006) Characterization of the global transcriptional responses of different types of DNA damage and disruption of replication in Bacillus subtilis. J Bacteriol 188:5595–5605.
Guariglia-Oropeza V.Helmann J.D.2011. Bacillus subtilis σV confers lysozyme resistance by activation of two cell wall modification pathways: peptidoglycan O-acetylation and D-alanylation of teichoic acidJ Bacteriol1936223-6232. Guariglia-Oropeza, V. and Helmann, J.D. (2011) Bacillus subtilis σV confers lysozyme resistance by activation of two cell wall modification pathways: peptidoglycan O-acetylation and D-alanylation of teichoic acid. J Bacteriol 193:6223–6232.
Hansson M.Hederstedt L.1992. Cloning and characterization of the Bacillus subtilis hemEHY gene cluster, which encodes protoheme IX biosynthetic enzymesJ Bacteriol1748081-8093. Hansson, M. and Hederstedt, L. (1992) Cloning and characterization of the Bacillus subtilis hemEHY gene cluster, which encodes protoheme IX biosynthetic enzymes. J Bacteriol 174:8081–8093.
Herbig A.Helmann J.D.2002. Metal ion and oxidative stressBacillus subtilis and Its Closest Relatives: From Genes to CellsSonenshein A.L.Hoch J.A.Losick R.ASM PressWashington DC405-414. Herbig, A. and Helmann, J.D. (2002) Metal ion and oxidative stress. In Bacillus subtilis and Its Closest Relatives: From Genes to Cells, edited by A.L. Sonenshein, J.A. Hoch, and R. Losick, ASM Press, Washington DC, pp 405–414.
Hesketh A.Hill C.Mokhtar J.Novotna G.Tran N.Bibb M.Hong H.-J.2011. Genome-wide dynamics of a bacterial response to antibiotics that target the cell envelopeBMC Genomics12e226. Hesketh, A., Hill, C., Mokhtar, J., Novotna, G., Tran, N., Bibb, M., and Hong, H.-J. (2011) Genome-wide dynamics of a bacterial response to antibiotics that target the cell envelope. BMC Genomics 12:e226, doi:10.1186/1471-2164-12-226.
Horneck G.Buecker H.Reitz G.Requardt H.Dose K.Martens K.D.Menningmann H.D.Weber P.1984. Microorganisms in the space environmentScience225226-228. Horneck, G., Buecker, H., Reitz, G., Requardt, H., Dose, K., Martens, K.D., Menningmann, H.D., and Weber, P. (1984) Microorganisms in the space environment. Science 225:226–228.
Horneck G.Buecker H.Reitz G.1994. Long-term survival of bacterial spores in spaceAdv Space Res1041-45. Horneck, G., Buecker, H., and Reitz, G. (1994) Long-term survival of bacterial spores in space. Adv Space Res 10:41–45.
Horneck G.Mileikowsky C.Melosh H.J.Wilson J.W.Cucinotta F.Gladman B.2002. Viable transfer of microorganisms in the Solar System and beyondAstrobiology, the Quest for the Conditions of LifeHorneck G.Baumstark-Khan C.SpringerBerlin57-74. Horneck, G., Mileikowsky, C., Melosh, H.J., Wilson, J.W., Cucinotta, F., and Gladman, B. (2002) Viable transfer of microorganisms in the Solar System and beyond. In Astrobiology, the Quest for the Conditions of Life, edited by G. Horneck and C. Baumstark-Khan, Springer, Berlin, pp 57–74.
Horneck G.Klaus D.M.Mancinelli R.L.2010. Space microbiologyMicrobiol Mol Biol Rev74121-156. Horneck, G., Klaus, D.M., and Mancinelli, R.L. (2010) Space microbiology. Microbiol Mol Biol Rev 74:121–156.
Horneck G.Moeller R.Cadet J.Douki T.Mancinelli R.L.Nicholson W.L.Panitz C.Rabbow E.Rettberg P.Spry A.Stackebrandt E.Vaishampayan P.Venkateswaran K.J.2012. Resistance of bacterial endospores to outer space for planetary protection purposes—experiment PROTECT of the EXPOSE-E missionAstrobiology12445-456. Horneck, G., Moeller, R., Cadet, J., Douki, T., Mancinelli, R.L., Nicholson, W.L., Panitz, C., Rabbow, E., Rettberg, P., Spry, A., Stackebrandt, E., Vaishampayan, P., and Venkateswaran, K.J. (2012) Resistance of bacterial endospores to outer space for planetary protection purposes—experiment PROTECT of the EXPOSE-E mission. Astrobiology 12:445–456.
Ibarra J.R.Orozco A.D.Rojas J.A.López K.Setlow P.Yasbin R.E.Pedraza-Reyes M.2008. Role of the Nfo and ExoA apurinic/apyrimidinic endoncleases in repair of DNA damage during outgrowth of Bacillus subtilis sporesJ Bacteriol1902031-2038. Ibarra, J.R., Orozco, A.D., Rojas, J.A., López, K., Setlow, P., Yasbin, R.E., and Pedraza-Reyes, M. (2008) Role of the Nfo and ExoA apurinic/apyrimidinic endoncleases in repair of DNA damage during outgrowth of Bacillus subtilis spores. J Bacteriol 190:2031–2038.
Jaenicke R.1981. Enzymes under extremes of physical conditionsAnnu Rev Biophys Bioeng101-67. Jaenicke, R. (1981) Enzymes under extremes of physical conditions. Annu Rev Biophys Bioeng 10:1–67.
Keijser B.J.F.Ter Beek A.Rauwerda H.Schuren F.Montijn R.van der Spek H.Brul S.2007. Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowthJ Bacteriol1893624-3634. Keijser, B.J.F., Ter Beek, A., Rauwerda, H., Schuren, F., Montijn, R., van der Spek, H., and Brul, S. (2007) Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowth. J Bacteriol 189:3624–3634.
Kempf M.J.Chen F.Kern R.Venkateswaran K.2005. Recurrent isolation of hydrogen-peroxide resistant spores of Bacillus pumilus from a spacecraft assembly facilityAstrobiology5391-405. Kempf, M.J., Chen, F., Kern, R., and Venkateswaran, K. (2005) Recurrent isolation of hydrogen-peroxide resistant spores of Bacillus pumilus from a spacecraft assembly facility. Astrobiology 5:391–405.
Kim H.Hahn M.Grabowski P.McPherson D.C.Otte M.M.Wang R.Ferguson C.C.Eichenberger P.Driks A.2006. The Bacillus subtilis spore coat protein interaction networkMol Microbiol59487-502. Kim, H., Hahn, M., Grabowski, P., McPherson, D.C., Otte, M.M., Wang, R., Ferguson, C.C., Eichenberger, P., and Driks, A. (2006) The Bacillus subtilis spore coat protein interaction network. Mol Microbiol 59:487–502.
Kooistra J.Haijema B.J.Venema G.1993. The Bacillus subtilis addAB genes are fully functional in Escherichia coliMol Microbiol7915-923. Kooistra, J., Haijema, B.J., and Venema, G. (1993) The Bacillus subtilis addAB genes are fully functional in Escherichia coli. Mol Microbiol 7:915–923.
Kunst F.Ogasawara N.Moszer I.Albertini A.M.Alloni G.Azevedo V.Bertero M.G.Bessières P.Bolotin A.Borchert S.Borriss R.Boursier L.Brans A.Braun M.Brignell S.C.Bron S.Brouillet S.Bruschi C.V.Caldwell B.Capuano V.Carter N.M.Choi S.-K.Codani J.-J.Connerton I.F.Cummings N.J.Daniel R.A.Denizot F.Devine K.M.Düsterhöft A.Ehrlich S.D.Emmerson P.T.Entian K.D.Errington J.Fabret C.Ferrari E.Foulger D.Fritz C.Fujita M.Fujita Y.Fuma S.Galizzi A.Galleron N.Ghim S.-Y.Glaser P.Goffeau A.Golightly E.J.Grandi G.Guiseppi G.Guy B.J.Haga K.Haiech J.Harwood C.R.Hénaut A.Hilbert H.Holsappel S.Hosono S.Hullo M.-F.Itaya M.Jones L.Joris B.Karamata D.Kasahara Y.Klaerr-Blanchard M.Klein C.Kobayashi Y.Koetter P.Koningstein G.Krogh S.Kumano M.Kurita K.Lapidus A.Lardinois S.Lauber J.Lazarevic V.Lee S.-M.Levine A.Liu H.Masuda S.Mauël C.Médigue C.Medina N.Mellado R.P.Mizuno M.Moestl D.Nakai S.Noback M.Noone D.O'Reilly M.Ogawa K.Ogiwara A.Oudega B.Park S.-H.Parro V.Pohl T.M.Portetelle D.Porwollik S.Prescott A.M.Presecan E.Pujic P.Purnelle B.Rapoport G.Rey M.Reynolds S.Rieger M.Rivolta C.Rocha E.Roche B.Rose M.Sadaie Y.Sato T.Scanlan E.Schleich S.Schroeter R.Scoffone F.Sekiguchi J.Sekowska A.Seror S.J.Serror P.Shin B.-S.Soldo B.Sorokin A.Tacconi E.Takagi T.Takahashi H.Takemaru K.Takeuchi M.Tamakoshi A.Tanaka T.Terpstra P.Tognoni A.Tosato V.Uchiyama S.Vandenbol M.Vannier F.Vassarotti A.Viari A.Wambutt R.Wedler E.Wedler H.Weitzenegger T.Winters P.Wipat A.Yamamoto H.Yamane K.Yasumoto K.Yata K.Yoshida K.Yoshikawa H.-F.Zumstein E.Yoshikawa H.Danchin A.1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilisNature390249-256. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., Bertero, M.G., Bessières, P., Bolotin, A., Borchert, S., Borriss, R., Boursier, L., Brans, A., Braun, M., Brignell, S.C., Bron, S., Brouillet, S., Bruschi, C.V., Caldwell, B., Capuano, V., Carter, N.M., Choi, S.-K., Codani, J.-J., Connerton, I.F., Cummings, N.J., Daniel, R.A., Denizot, F., Devine, K.M., Düsterhöft, A., Ehrlich, S.D., Emmerson, P.T., Entian, K.D., Errington, J., Fabret, C., Ferrari, E., Foulger, D., Fritz, C., Fujita, M., Fujita, Y., Fuma, S., Galizzi, A., Galleron, N., Ghim, S.-Y., Glaser, P., Goffeau, A., Golightly, E.J., Grandi, G., Guiseppi, G., Guy, B.J., Haga, K., Haiech, J., Harwood, C.R., Hénaut, A., Hilbert, H., Holsappel, S., Hosono, S., Hullo, M.-F., Itaya, M., Jones, L., Joris, B., Karamata, D., Kasahara, Y., Klaerr-Blanchard, M., Klein, C., Kobayashi, Y., Koetter, P., Koningstein, G., Krogh, S., Kumano, M., Kurita, K., Lapidus, A., Lardinois, S., Lauber, J., Lazarevic, V., Lee, S.-M., Levine, A., Liu, H., Masuda, S., Mauël, C., Médigue, C., Medina, N., Mellado, R.P., Mizuno, M., Moestl, D., Nakai, S., Noback, M., Noone, D., O'Reilly, M., Ogawa, K., Ogiwara, A., Oudega, B., Park, S.-H., Parro, V., Pohl, T.M., Portetelle, D., Porwollik, S., Prescott, A.M., Presecan, E., Pujic, P., Purnelle, B., Rapoport, G., Rey, M., Reynolds, S., Rieger, M., Rivolta, C., Rocha, E., Roche, B., Rose, M., Sadaie, Y., Sato, T., Scanlan, E., Schleich, S., Schroeter, R., Scoffone, F., Sekiguchi, J., Sekowska, A., Seror, S.J., Serror, P., Shin, B.-S., Soldo, B., Sorokin, A., Tacconi, E., Takagi, T., Takahashi, H., Takemaru, K., Takeuchi, M., Tamakoshi, A., Tanaka, T., Terpstra, P., Tognoni, A., Tosato, V., Uchiyama, S., Vandenbol, M., Vannier, F., Vassarotti, A., Viari, A., Wambutt, R., Wedler, E., Wedler, H., Weitzenegger, T., Winters, P., Wipat, A., Yamamoto, H., Yamane, K., Yasumoto, K., Yata, K., Yoshida, K., Yoshikawa, H.-F., Zumstein, E., Yoshikawa, H., and Danchin, A. (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249–256.
Lindberg C.Horneck G.1991. Action spectra for survival and spore photoproduct formation of Bacillus subtilis irradiated with short-wavelength (200–300 nm) UV at atmospheric pressure and in vacuoJ Photochem Photobiol B Biol1169-80. Lindberg, C. and Horneck, G. (1991) Action spectra for survival and spore photoproduct formation of Bacillus subtilis irradiated with short-wavelength (200–300 nm) UV at atmospheric pressure and in vacuo. J Photochem Photobiol B Biol 11:69–80.
Link L.Sawyer J.Venkateswaran K.Nicholson W.L.2004. Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facilityMicrob Ecol47159-163. Link, L., Sawyer, J., Venkateswaran, K., and Nicholson, W.L. (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microb Ecol 47:159–163.
Mascarenhas J.Sanchez H.Tadesse S.Kidane D.Krisnamurthy M.Alonso J.C.Graumann P.L.2006. Bacillus subtilis SbcC protein plays an important role in DNA inter-strand cross-link repairBMC Mol Biol7e20. Mascarenhas, J., Sanchez, H., Tadesse, S., Kidane, D., Krisnamurthy, M., Alonso, J.C., and Graumann, P.L. (2006) Bacillus subtilis SbcC protein plays an important role in DNA inter-strand cross-link repair. BMC Mol Biol 7:e20, doi:10.1186/1471-2199-7-20.
Miethke M.Hecker M.Gerth U.2006. Involvement of Bacillus subtilis ClpE in CtsR degradation and protein quality controlJ Bacteriol1884610-4619. Miethke, M., Hecker, M., and Gerth, U. (2006) Involvement of Bacillus subtilis ClpE in CtsR degradation and protein quality control. J Bacteriol 188:4610–4619.
Miller J.M.1972Experiments in Molecular GeneticsASM PressWashington DC. Miller, J.M. (1972) Experiments in Molecular Genetics, ASM Press, Washington DC.
Miron M.Woody O.Z.Marcil A.Murie C.Sladek R.Nadon R.2006. A methodology for global validation of microarray experimentsBMC Bioinformatics7e333. Miron, M., Woody, O.Z., Marcil, A., Murie, C., Sladek, R., and Nadon, R. (2006) A methodology for global validation of microarray experiments. BMC Bioinformatics 7:e333, doi:10.1186/1471-2105-7-333.
Moeller R.Stackebrandt E.Reitz G.Rettberg P.Doherty A.J.Horneck G.Nicholson W.L.2007. Role of DNA repair by non-homologous end joining in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV and ionizing radiationJ Bacteriol1893306-3311. Moeller, R., Stackebrandt, E., Reitz, G., Rettberg, P., Doherty, A.J., Horneck, G., and Nicholson, W.L. (2007) Role of DNA repair by non-homologous end joining in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV and ionizing radiation. J Bacteriol 189:3306–3311.
Moeller R.Schuerger A.C.Reitz G.Nicholson W.L.2011. Impact of two DNA repair pathways, homologous recombination and non-homologous end joining, on bacterial spore inactivation under simulated martian environmental conditionsIcarus215204-210. Moeller, R., Schuerger, A.C., Reitz, G., and Nicholson, W.L. (2011) Impact of two DNA repair pathways, homologous recombination and non-homologous end joining, on bacterial spore inactivation under simulated martian environmental conditions. Icarus 215:204–210.
Moeller R.Reitz G.Nicholson W.L.Cadet J.Douki T.Mancinelli R.L.Panitz C.Rabbow E.Rettberg P.Spry A.Stackebrandt E.Vaishampayan P.Venkateswaran K.J.Horneck G.2012. Mutagenesis in bacterial spores exposed to space and simulated martian conditions: data from the EXPOSE-E spaceflight experiment PROTECTAstrobiology12457-468. Moeller, R., Reitz, G., Nicholson, W.L., Cadet, J., Douki, T., Mancinelli, R.L., Panitz, C., Rabbow, E., Rettberg, P., Spry, A., Stackebrandt, E., Vaishampayan, P., Venkateswaran, K.J., and Horneck, G. (2012) Mutagenesis in bacterial spores exposed to space and simulated martian conditions: data from the EXPOSE-E spaceflight experiment PROTECT. Astrobiology 12:457–468.
Morey J.S.Ryan J.C.Van Dolah F.M.2006. Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCRBiol Proced Online8175-193. Morey, J.S., Ryan, J.C., and Van Dolah, F.M. (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8:175–193.
Nicholson W.L.2003. Using thermal inactivation kinetics to determinine bacterial spore longevity: implications for paleomicrobiology and lithopanspermiaOrig Life Evol Biosph33621-631. Nicholson, W.L. (2003) Using thermal inactivation kinetics to determinine bacterial spore longevity: implications for paleomicrobiology and lithopanspermia. Orig Life Evol Biosph 33:621–631.
Nicholson W.L.Setlow P.1990. Sporulation, germination, and outgrowthMolecular Biological Methods for BacillusHarwood C.R.Cutting S.M.John Wiley & SonsSussex, England391-450. Nicholson, W.L. and Setlow, P. (1990) Sporulation, germination, and outgrowth. In Molecular Biological Methods for Bacillus, edited by C.R. Harwood and S.M. Cutting, John Wiley & Sons, Sussex, England, pp 391–450.
Nicholson W.L.Munakata N.Horneck G.Melosh H.J.Setlow P.2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environmentsMicrobiol Mol Biol Rev64548-572. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J., and Setlow, P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572.
Nicholson W.L.Schuerger A.C.Setlow P.2005. The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflightMutat Res571249-264. Nicholson, W.L., Schuerger, A.C., and Setlow, P. (2005) The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat Res 571:249–264.
Nicholson W.L.Schuerger A.C.Race M.S.2009. Migrating microbes and planetary protectionTrends Microbiol17389-392. Nicholson, W.L., Schuerger, A.C., and Race, M.S. (2009) Migrating microbes and planetary protection. Trends Microbiol 17:389–392.
Ozin A.J.Henriques A.O.Yi H.Moran C.P. Jr2000. Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coatJ Bacteriol1821828-1833. Ozin, A.J., Henriques, A.O., Yi, H., and Moran, C.P., Jr. (2000) Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coat. J Bacteriol 182:1828–1833.
Pedersen L.B.Setlow P.2000. Penicillin-binding protein-related factor A is required for proper chromosome segregation in Bacillus subtilisJ Bacteriol1821650-1658. Pedersen, L.B. and Setlow, P. (2000) Penicillin-binding protein-related factor A is required for proper chromosome segregation in Bacillus subtilis. J Bacteriol 182:1650–1658.
Pedersen L.B.Angert E.R.Setlow P.1999. Septal localization of penicillin-binding protein 1 in Bacillus subtilisJ Bacteriol1813201-3211. Pedersen, L.B., Angert, E.R., and Setlow, P. (1999) Septal localization of penicillin-binding protein 1 in Bacillus subtilis. J Bacteriol 181:3201–3211.
Perkins A.E.Schuerger A.C.Nicholson W.L.2008. Isolation of rpoB mutations causing rifampicin resistance in Bacillus subtilis spores exposed to simulated martian surface conditionsAstrobiology81159-1167. Perkins, A.E., Schuerger, A.C., and Nicholson, W.L. (2008) Isolation of rpoB mutations causing rifampicin resistance in Bacillus subtilis spores exposed to simulated martian surface conditions. Astrobiology 8:1159–1167.
Pottathil M.Lazazzera B.A.2003. The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilisFront Biosci8D32-D45. Pottathil, M. and Lazazzera, B.A. (2003) The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 8:D32–D45.
Rabbow E.Rettberg P.Barczyk S.Bohmeier M.Parpart A.Panitz C.Horneck G.von Heise-Rotenburg R.Hoppenbrouwers T.Willnecker R.Baglioni P.Demets R.Dettmann J.Reitz G.2012. EXPOSE-E: an ESA astrobiology mission 1.5 years in spaceAstrobiology12374-386. Rabbow, E., Rettberg, P., Barczyk, S., Bohmeier, M., Parpart, A., Panitz, C., Horneck, G., von Heise-Rotenburg, R., Hoppenbrouwers, T., Willnecker, R., Baglioni, P., Demets, R., Dettmann, J., and Reitz, G. (2012) EXPOSE-E: an ESA astrobiology mission 1.5 years in space. Astrobiology 12:374–386.
Rivas-Castillo A.M.Yasbin R.E.Robleto E.Nicholson W.L.Pedraza-Reyes M.2010. Role of the Y-family DNA polymerases YqjH and YqjW in protecting sporulating Bacillus subtilis cells from DNA damageCurr Microbiol60263-267. Rivas-Castillo, A.M., Yasbin, R.E., Robleto, E., Nicholson, W.L., and Pedraza-Reyes, M. (2010) Role of the Y-family DNA polymerases YqjH and YqjW in protecting sporulating Bacillus subtilis cells from DNA damage. Curr Microbiol 60:263–267.
Roels S.Losick R.1995. Adjacent and divergently oriented operons under the control of the sporulation regulatory protein gerE in Bacillus subtilisJ Bacteriol1776263-6275. Roels, S. and Losick, R. (1995) Adjacent and divergently oriented operons under the control of the sporulation regulatory protein gerE in Bacillus subtilis. J Bacteriol 177:6263–6275.
Rummel J.D.2001. Planetary protection in the time of astrobiology: protecting against biological contaminationProc Natl Acad Sci USA982128-2131. Rummel, J.D. (2001) Planetary protection in the time of astrobiology: protecting against biological contamination. Proc Natl Acad Sci USA 98:2128–2131.
Sanchez H.Kidane D.Reed P.Curtis F.A.Cozar M.C.Graumann P.L.Sharples G.Alonso J.C.2005. The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilisGenetics171873-883. Sanchez, H., Kidane, D., Reed, P., Curtis, F.A., Cozar, M.C., Graumann, P.L., Sharples, G., and Alonso, J.C. (2005) The RuvAB branch migration translocase and RecU Holliday junction resolvase are required for double-stranded DNA break repair in Bacillus subtilis. Genetics 171:873–883.
Satomi M.La Duc M.T.Venkateswaran K.2006. Bacillus safensis sp. nov., isolated from spacecraft and assembly-facility surfacesInt J Syst Evol Microbiol561735-1740. Satomi, M., La Duc, M.T., and Venkateswaran, K. (2006) Bacillus safensis sp. nov., isolated from spacecraft and assembly-facility surfaces. Int J Syst Evol Microbiol 56:1735–1740.
Schaeffer P.Millet J.Aubert J.-P.1965. Catabolic repression of bacterial sporulationProc Natl Acad Sci USA54704-711. Schaeffer, P., Millet, J., and Aubert, J.-P. (1965) Catabolic repression of bacterial sporulation. Proc Natl Acad Sci USA 54:704–711.
Schuerger A.C.Mancinelli R.L.Kern R.G.Rothschild L.J.McKay C.P.2003. Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: implications for the forward contamination of MarsIcarus165253-276. Schuerger, A.C., Mancinelli, R.L., Kern, R.G., Rothschild, L.J., and McKay, C.P. (2003) Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: implications for the forward contamination of Mars. Icarus 165:253–276.
Schuerger A.C.Richards J.T.Newcombe D.A.Venkateswaran K.2006. Rapid inactivation of seven Bacillus sppunder simulated Mars UV irradiation. Icarus18152-62. Schuerger, A.C., Richards, J.T., Newcombe, D.A., and Venkateswaran, K. (2006) Rapid inactivation of seven Bacillus spp. under simulated Mars UV irradiation. Icarus 181:52–62.
Schumann W.2003. The Bacillus subtilis heat shock stimulonCell Stress Chaperones8207-217. Schumann, W. (2003) The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 8:207–217.
Setlow P.2007. I will survive: DNA protection in bacterial sporesTrends Microbiol15172-180. Setlow, P. (2007) I will survive: DNA protection in bacterial spores. Trends Microbiol 15:172–180.
Sharples G.J.Lloyd R.G.1993. Location of the Bacillus subtilis sbcD gene downstream of addAB, the analogs of Escherichia coli recBCNucleic Acids Res212010. Sharples, G.J. and Lloyd, R.G. (1993) Location of the Bacillus subtilis sbcD gene downstream of addAB, the analogs of Escherichia coli recBC. Nucleic Acids Res 21:2010.
Simmons L.A.Goranov A.I.Kobayashi H.Davies B.W.Yuan D.S.Grossman A.D.Walker G.C.2009. Comparison of responses to double-strand breaks between Escherichia coli and Bacillus subtilis reveals different requirements for SOS inductionJ Bacteriol1911152-1161. Simmons, L.A., Goranov, A.I., Kobayashi, H., Davies, B.W., Yuan, D.S., Grossman, A.D., and Walker, G.C. (2009) Comparison of responses to double-strand breaks between Escherichia coli and Bacillus subtilis reveals different requirements for SOS induction. J Bacteriol 191:1152–1161.
Sonenshein A.L.Hoch J.A.Losick R.2002. Appendix 1: general view of the Bacillus subtilis chromosomeBacillus subtilis and Its Closest Relatives: From Genes to CellsASM PressWashington DC552-569. Sonenshein, A.L., Hoch, J.A., and Losick, R., editors. (2002) Appendix 1: general view of the Bacillus subtilis chromosome. In Bacillus subtilis and Its Closest Relatives: From Genes to Cells, ASM Press, Washington DC, pp 552–569.
Storz G.Hengge R.2011Bacterial Stress ResponsesASM PressWashington DC. Storz, G. and Hengge, R. (2011) Bacterial Stress Responses, ASM Press, Washington DC.
Sung H.-M.Yeamans G.Ross C.A.Yasbin R.E.2003. Roles of YqjH and YqjW, homologs of the Escherichia coli UmuC/DinB or Y superfamily of DNA polymerases, in stationary-phase mutagenesis and UV-induced mutagenesis of Bacillus subtilisJ Bacteriol1852153-2160. Sung, H.-M., Yeamans, G., Ross, C.A., and Yasbin, R.E. (2003) Roles of YqjH and YqjW, homologs of the Escherichia coli UmuC/DinB or Y superfamily of DNA polymerases, in stationary-phase mutagenesis and UV-induced mutagenesis of Bacillus subtilis. J Bacteriol 185:2153–2160.
Tam L.T.Antelmann H.Eymann C.Albrecht D.Bernhardt J.Hecker M.2006. Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2-D gel image color coding approachProteomics64565-4585. Tam, L.T., Antelmann, H., Eymann, C., Albrecht, D., Bernhardt, J., and Hecker, M. (2006) Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2-D gel image color coding approach. Proteomics 6:4565–4585.
United Nations1967Treaty on principles governing the activities of states in the exploration and use of outer space, including the Moon and other celestial bodieshttp://www.state.gov/t/isn/5181.htm. United Nations. (1967) Treaty on principles governing the activities of states in the exploration and use of outer space, including the Moon and other celestial bodies. Available online at http://www.state.gov/t/isn/5181.htm.
Vyas J.Cox J.Setlow B.Coleman W.H.Setlow P.2011. Extremely variable conservation of gamma-type small, acid-soluble proteins from spores of some species in the bacterial order BacillalesJ Bacteriol1931884-1892. Vyas, J., Cox, J., Setlow, B., Coleman, W.H., and Setlow, P. (2011) Extremely variable conservation of gamma-type small, acid-soluble proteins from spores of some species in the bacterial order Bacillales. J Bacteriol 193:1884–1892.
Yasbin R.E.Cheo D.Bol D.1993. DNA repair systemsBacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular GeneticsSonenshein A.L.Hoch J.A.Losick R.ASM PressWashington DC529-537. Yasbin, R.E., Cheo, D., and Bol, D. (1993) DNA repair systems. In Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics, edited by A.L. Sonenshein, J.A. Hoch, and R. Losick, ASM Press, Washington DC, pp 529–537.
Yeeles J.T.P.van Aelst K.Dillingham M.S.Moreno-Herrero F.2011. Recombination hotspots and single-stranded DNA binding proteins couple DNA translocation to DNA unwinding by the AddAB helicase-nucleaseMol Cell42806-816. Yeeles, J.T.P., van Aelst, K., Dillingham, M.S., and Moreno-Herrero, F. (2011) Recombination hotspots and single-stranded DNA binding proteins couple DNA translocation to DNA unwinding by the AddAB helicase-nuclease. Mol Cell 42:806–816.
Zahler S.A.1993. Temperate bacteriophagesBacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular GeneticsSonenshein A.L.Hoch J.A.Losick R.ASM PressWashington DC831-842. Zahler, S.A. (1993) Temperate bacteriophages. In Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics, edited by A.L. Sonenshein, J.A. Hoch, and R. Losick, ASM Press, Washington DC, pp 831–842.
Zeigler D.R.Prágai Z.Rodriguez S.Chevreux B.Muffler A.Albert T.Bai R.Wyss M.Perkins J.B.2008. The origins of 168, W23, and other Bacillus subtilis legacy strainsJ Bacteriol1906983-6995. Zeigler, D.R., Prágai, Z., Rodriguez, S., Chevreux, B., Muffler, A., Albert, T., Bai, R., Wyss, M., and Perkins, J.B. (2008) The origins of 168, W23, and other Bacillus subtilis legacy strains. J Bacteriol 190:6983–6995.
Information & Authors
Information
Published In
Copyright
Copyright 2012, Mary Ann Liebert, Inc.
History
Published online: 8 June 2012
Published in print: May 2012
Accepted: 14 April 2012
Received: 10 October 2011
Topics
Authors
Author Disclosure Statement
No competing financial interests exist.
Metrics & Citations
Metrics
Citations
Export Citation
Export citation
Select the format you want to export the citations of this publication.
View Options
Get Access
Access content
To read the fulltext, please use one of the options below to sign in or purchase access.⚠ Society Access
If you are a member of a society that has access to this content please log in via your society website and then return to this publication.