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Origins of Life and Evolution of Biospheres

, Volume 44, Issue 3, pp 209–221 | Cite as

Detection of Macromolecules in Desert Cyanobacteria Mixed with a Lunar Mineral Analogue After Space Simulations

  • Mickael Baqué
  • Cyprien Verseux
  • Elke Rabbow
  • Jean-Pierre Paul de Vera
  • Daniela BilliEmail author
Astrobiology

Abstract

In the context of future exposure missions in Low Earth Orbit and possibly on the Moon, two desert strains of the cyanobacterium Chroococcidiopsis, strains CCMEE 029 and 057, mixed or not with a lunar mineral analogue, were exposed to fractionated fluencies of UVC and polychromatic UV (200–400 nm) and to space vacuum. These experiments were carried out within the framework of the BIOMEX (BIOlogy and Mars EXperiment) project, which aims at broadening our knowledge of mineral-microorganism interaction and the stability/degradation of their macromolecules when exposed to space and simulated Martian conditions. The presence of mineral analogues provided a protective effect, preserving survivability and integrity of DNA and photosynthetic pigments, as revealed by testing colony-forming abilities, performing PCR-based assays and using confocal laser scanning microscopy. In particular, DNA and pigments were still detectable after 500 kJ/m2 of polychromatic UV and space vacuum (10−4 Pa), corresponding to conditions expected during one-year exposure in Low Earth Orbit on board the EXPOSE-R2 platform in the presence of 0.1 % Neutral Density (ND) filter. After exposure to high UV fluencies (800 MJ/m2) in the presence of minerals, however, altered fluorescence emission spectrum of the photosynthetic pigments were detected, whereas DNA was still amplified by PCR. The present paper considers the implications of such findings for the detection of biosignatures in extraterrestrial conditions and for putative future lunar missions.

Keywords

Astrobiology Extreme environments Expose-R2 Biosignatures Lunar regolith 

Notes

Acknowledgments

This research was funded by the Italian Space Agency (contract ASI-2013-051-R.0 to DB) and supported by the German Helmholtz Association through the Helmholtz-Alliance “Planetary Evolution and Life”. The authors thank Dr. Elena Romano, Centre of Advanced Microscopy “Patrizia Albertano”, Tor Vergata University, for her skillful assistance in using the CLSM facility.

References

  1. Armstrong J, Wells L, Gonzalez G (2002) Rummaging through earth’s attic for remains of ancient life. Icarus 160:183–196. doi: 10.1006/icar.2002.6957 CrossRefGoogle Scholar
  2. Bahl J, Lau MCY, Smith GJD, Vijaykrishna D, Cary SC, Lacap DC, Lee CK, Papke RT, Warren-Rhodes KA, Wong FKY, McKay CP, Pointing SB (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:163. doi: 10.1038/ncomms1167 PubMedCentralPubMedCrossRefGoogle Scholar
  3. Baqué M, de Vera J-P, Rettberg P, Billi D (2013a) The BOSS and BIOMEX space experiments on the EXPOSE-R2 mission: endurance of the desert cyanobacterium Chroococcidiopsis under simulated space vacuum, Martian atmosphere, UVC radiation and temperature extremes. Acta Astronaut 91:180–186. doi: 10.1016/j.actaastro.2013.05.015 CrossRefGoogle Scholar
  4. Baqué M, Viaggiu E, Scalzi G, Billi D (2013b) Endurance of the endolithic desert cyanobacterium Chroococcidiopsis under UVC radiation. Extremophiles 17:161–169. doi: 10.1007/s00792-012-0505-5 PubMedCrossRefGoogle Scholar
  5. Barnes D, Battistelli E, Bertrand R, Butera F, Chatila R, Del Biancio A, Draper C, Ellery A, Gelmi R, Ingrand F, Koeck C, Lacroix S, Lamon P, Lee C, Magnani P, Patel N, Pompei C, Re E, Richter L, Rowe M, Siegwart R, Slade R, Smith MF, Terrien G, Wall R, Ward R, Waugh L, Woods M (2006) The ExoMars rover and Pasteur payload phase a study: an approach to experimental astrobiology. Int J Astrobiol 5:221–241. doi: 10.1017/S1473550406003090 CrossRefGoogle Scholar
  6. Billi D, Friedmann EI, Hofer KG, Grilli Caiola M, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. J Appl Environ Microbiol 66:1489–1492. doi: 10.1128/aem.66.4.1489-1492.2000 CrossRefGoogle Scholar
  7. Billi D, Viaggiu E, Cockell CS, Rabbow E, Horneck G, Onofri S (2011) Damage escape and repair in dried Chroococcidiopsis spp. from hot and cold deserts exposed to simulated space and Martian conditions. Astrobiology 1:65–73. doi: 10.1089/ast.2009.0430 CrossRefGoogle Scholar
  8. Carpenter JD, Fisackerly R, De Rosa D, Houdou B (2012) Scientific preparations for lunar exploration with the European Lunar lander. Planet Space Sci 74:208–223. doi: 10.1016/j.pss.2012.07.024 CrossRefGoogle Scholar
  9. Carr CE, Rowedder H, Vafadari C, Lui CS, Cascio E, Zuber MT, Ruvkun G (2013) Radiation resistance of biological reagents for in situ life detection. Astrobiology 13:68–78. doi: 10.1089/ast.2012.0869 PubMedCrossRefGoogle Scholar
  10. Cockell CS, Catling DC, Davis WL, Snook K, Kepner RL, Lee P, McKay CP (2000) The ultraviolet environment of mars: biological implications past, present, and future. Icarus 146:343–359. doi: 10.1006/icar.2000.6393 PubMedCrossRefGoogle Scholar
  11. Cockell CS, Schuerger AC, Billi D, Friedmann EI, Panitz C (2005) Effects of a simulated Martian UV flux on the cyanobacterium, Chroococcidiopsis sp. 029. Astrobiology 5:127–140. doi: 10.1089/ast.2005.5.127 PubMedCrossRefGoogle Scholar
  12. Crawford IA, Anand M, Cockell CS, Falcke H, Green DA, Jaumann R, Wieczorek MA (2012) Back to the moon: the scientific rationale for resuming lunar surface exploration. Planet Space Sci 74:3–14. doi: 10.1016/j.pss.2012.06.002 CrossRefGoogle Scholar
  13. Daly MJ (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7:237–245. doi: 10.1038/nrmicro2073 PubMedCrossRefGoogle Scholar
  14. Dartnell LR, Patel MR (2013) Degradation of microbial fluorescence biosignatures by solar ultraviolet radiation on Mars. Int J Astrobiol 13:112–123. doi: 10.1017/S1473550413000335 CrossRefGoogle Scholar
  15. Dartnell LR, Storrie-Lombardi MC, Mullineaux CW, Ruban AV, Wright G, Griffiths AD, Muller J-P, Ward JM (2011) Degradation of cyanobacterial biosignatures by ionizing radiation. Astrobiology 11:997–1016. doi: 10.1089/ast.2011.0663 PubMedCrossRefGoogle Scholar
  16. De Vera J-P, Boettger U, Noetzel RDLT, Sánchez FJ, Grunow D, Schmitz N, Lange C, Hübers H-W, Billi D, Baqué M, Rettberg P, Rabbow E, Reitz G, Berger T, Möller R, Bohmeier M, Horneck G, Westall F, Jänchen J, Fritz J, Meyer C, Onofri S, Selbmann L, Zucconi L, Kozyrovska N, Leya T, Foing B, Demets R, Cockell CS, Bryce C, Wagner D, Serrano P, Edwards HGM, Joshi J, Huwe B, Ehrenfreund P, Elsaesser A, Ott S, Meessen J, Feyh N, Szewzyk U, Jaumann R, Spohn T (2012) Supporting mars exploration: BIOMEX in low earth orbit and further astrobiological studies on the moon using Raman and PanCam technology. Planet Space Sci 74:103–110. doi: 10.1016/j.pss.2012.06.010 CrossRefGoogle Scholar
  17. Demets R, Schulte W, Baglioni P (2005) The past, present and future of Biopan. Adv Space Res 36:311–316. doi: 10.1016/j.asr.2005.07.005 CrossRefGoogle Scholar
  18. Direito SOL, Marees A, Röling WFM (2012) Sensitive life detection strategies for low-biomass environments: optimizing extraction of nucleic acids adsorbing to terrestrial and Mars analogue minerals. FEMS Microbiol Ecol 81:111–123. doi: 10.1111/j.1574-6941.2012.01325.x PubMedCrossRefGoogle Scholar
  19. Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Orig Life 10:223–235. doi: 10.1007/BF00928400 PubMedCrossRefGoogle Scholar
  20. Hansen AA, Jensen LL, Kristoffersen T, Mikkelsen K, Merrison J, Finster KW, Lomstein BA (2009) Effects of long-term simulated Martian conditions on a freeze-dried and homogenized bacterial permafrost community. Astrobiology 9:229–240. doi: 10.1089/ast.2008.0244 PubMedCrossRefGoogle Scholar
  21. Isenbarger TA, Carr CE, Johnson SS, Finney M, Church GM, Gilbert W, Zuber MT, Ruvkun G (2008) The most conserved genome segments for life detection on earth and other planets. Orig Life Evol Biosph 38:517–533. doi: 10.1007/s11084-008-9148-z PubMedCrossRefGoogle Scholar
  22. Kozyrovska NO, Lutvynenko TL, Korniichuk OS, Kovalchuk MV, Voznyuk TM, Kononuchenko O, Zaetz I, Rogutskyy I, Mytrokhyn OV, Mashkovska SP, Foing BH, Kordyum VA (2006) Growing pioneer plants for a lunar base. Adv Space Res 37:93–99. doi: 10.1016/j.asr.2005.03.005 CrossRefGoogle Scholar
  23. Mahaffy PR, Webster CR, Cabane M, Conrad PG, Coll P, Atreya SK, Arvey R, Barciniak M, Benna M, Bleacher L, Brinckerhoff WB, Eigenbrode JL, Carignan D, Cascia M, Chalmers RA, Dworkin JP, Errigo T, Everson P, Franz H, Farley R, Feng S, Frazier G, Freissinet C, Glavin DP, Harpold DN, Hawk D, Holmes V, Johnson S, Jones A, Jordan P, Kellogg J, Lewis J, Lyness E, Malespin CA, Martin DK, Maurer J, McAdam AC, McLennan D, Nolan TJ, Noriega M, Pavlov AA, Prats B, Raaen E, Sheinman O, Sheppard D, Smith J, Stern JC, Tan F, Trainer M, Ming DW, Morris RV, Jones J, Gundersen C, Steele A, Wray J, Botta O, Leshin LA, Owen T, Battel S, Jakosky BM, Manning H, Squyres S, Navarro-González R, McKay CP, Raulin F, Sternberg R, Buch A, Sorensen P, Kline-Schoder R, Coscia D, Szopa C, Teinturier S, Baffes C, Feldman J, Flesch G, Forouhar S, Garcia R, Keymeulen D, Woodward S, Block BP, Arnett K, Miller R, Edmonson C, Gorevan S, Mumm E (2012) The sample analysis at Mars investigation and instrument suite. Space Sci Rev 170:401–478. doi: 10.1007/s11214-012-9879-z CrossRefGoogle Scholar
  24. McKay CP, Stoker CR, Glass BJ, Davé AI, Davila AF, Heldmann JL, Marinova MM, Fairen AG, Quinn RC, Zacny KA, Paulsen G, Smith PH, Parro V, Andersen DT, Hecht MH, Lacelle D, Pollard WH (2013) The Icebreaker life mission to mars: a search for biomolecular evidence for life. Astrobiology 13:334–353. doi: 10.1089/ast.2012.0878 PubMedCrossRefGoogle Scholar
  25. Montague M, McArthur GH, Cockell CS, Held J, Marshall W, Sherman LA, Wang N, Nicholson WL, Tarjan DR, Cumbers J (2012) The role of synthetic biology for in situ resource utilization (ISRU). Astrobiology 12:1135–1142. doi: 10.1089/ast.2012.0829 PubMedCrossRefGoogle Scholar
  26. Mytrokhyn OV, Bogdanova SV, Shumlyanskyy LV (2003) Anorthosite rocks of fedorivskyy suite (Korosten Pluton, Ukrainian Shield). Current problems in geology. Kyiv National University, Kyiv, pp 53–57Google Scholar
  27. Olsson-Francis K, Cockell CS (2010) Use of cyanobacteria for in-situ resource use in space applications. Planet Space Sci 58:1279–1285. doi: 10.1016/j.pss.2010.05.005 CrossRefGoogle Scholar
  28. Parnell J, Cullen D, Sims MR, Bowden S, Cockell CS, Court R, Ehrenfreund P, Gaubert F, Grant W, Parro V, Rohmer M, Sephton M, Stan-Lotter H, Steele A, Toporski J, Vago J (2007) Searching for life on mars: selection of molecular targets for ESA’s Aurora ExoMars mission. Astrobiology 7:578–604. doi: 10.1089/ast.2006.0110 PubMedCrossRefGoogle Scholar
  29. Parro V, Rivas LA, Gómez-Elvira J (2008) Protein microarrays-based strategies for life detection in astrobiology. Space Sci Rev 135:293–311. doi: 10.1007/s11214-007-9276-1 CrossRefGoogle Scholar
  30. Parro V, de Diego-Castilla G, Rodríguez-Manfredi JA, Rivas LA, Blanco-López Y, Sebastián E, Romeral J, Compostizo C, Herrero PL, García-Marín A, Moreno-Paz M, García-Villadangos M, Cruz-Gil P, Peinado V, Martín-Soler J, Pérez-Mercader J, Gómez-Elvira J (2011) SOLID3: a multiplex antibody microarray-based optical sensor instrument for in situ life detection in planetary exploration. Astrobiology 11:15–28. doi: 10.1089/ast.2010.0501 PubMedCrossRefGoogle Scholar
  31. Patel MR, Bérces A, Kerékgyárto T, Rontó G, Lammer H, Zarnecki JC (2004) Annual solar UV exposure and biological effective dose rates on the Martian surface. Adv Space Res 33:1247–1252. doi: 10.1016/j.asr.2003.08.036 PubMedCrossRefGoogle Scholar
  32. Rabbow E, Horneck G, Rettberg P, Schott J-U, Panitz C, L’Afflitto A, von Heise-Rotenburg R, Willnecker R, Baglioni P, Hatton J, Dettmann J, Demets R, Reitz G (2009) EXPOSE, an astrobiological exposure facility on the international space station - from proposal to flight. Orig Life Evol Biosph 39:581–598PubMedCrossRefGoogle Scholar
  33. 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 space. Astrobiology 12:374–386. doi: 10.1089/ast.2011.0760 PubMedCrossRefGoogle Scholar
  34. Roldán M, Thomas F, Castel S, Quesada A, Hernández-Mariné M (2004) Noninvasive pigment identification in single cells from living phototrophic biofilms by confocal imaging spectrofluorometry. J Appl Environ Microbiol 70:3745–3750. doi: 10.1128/AEM.70.6.3745-3750.2004 CrossRefGoogle Scholar
  35. Schulze-Makuch D (2013) Organic molecules in lunar ice: A window to the early evolution of life on Earth. In: de Vera JP, Seckbach J (eds) Cellular origins, life in extreme habitats and astrobiology vol 28, Habitability of other planets and satellites Springer Netherlands, pp 333–345. doi: 10.1007/978-94-007-6546-7-7
  36. Sims MR, Cullen DC, Rix CS, Buckley A, Derveni M, Evans D, Miguel García-Con L, Rhodes A, Rato CC, Stefinovic M, Sephton MA, Court RW, Bulloch C, Kitchingman I, Ali Z, Pullan D, Holt J, Blake O, Sykes J, Samara-Ratna P, Canali M, Borst G, Leeuwis H, Prak A, Norfini A, Geraci E, Tavanti M, Brucato J, Holm N (2012) Development status of the life marker chip instrument for ExoMars. Planet Space Sci 72:129–137. doi: 10.1016/j.pss.2012.04.007 CrossRefGoogle Scholar
  37. Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191. doi: 10.1128/MMBR.00015-10 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Vago J, Gardini B, Kminek G, Baglioni P, Gianfiglio G, Santovincenzo A, Bayón S, van Winnendael M (2006) ExoMars - searching for life on the red planet. ESA Bull 126:16–23Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Mickael Baqué
    • 1
  • Cyprien Verseux
    • 1
  • Elke Rabbow
    • 3
  • Jean-Pierre Paul de Vera
    • 2
  • Daniela Billi
    • 1
    Email author
  1. 1.Department of BiologyUniversity of Rome “Tor Vergata”RomeItaly
  2. 2.Institute of Planetary ResearchGerman Aerospace Center (DLR) BerlinBerlinGermany
  3. 3.Radiation Biology Department, Institute of Aerospace MedicineGerman Aerospace Center (DLR)CologneGermany

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