Skip to main content Accessibility help
×
Home
Hostname: page-component-5cfd469876-gzklw Total loading time: 0.345 Render date: 2021-06-25T02:11:56.480Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true }

Exposure to low Earth orbit of an extreme-tolerant cyanobacterium as a contribution to lunar astrobiology activities

Published online by Cambridge University Press:  18 July 2019

Daniela Billi
Affiliation:
Department of Biology, University of Rome Tor Vergata, Rome, Italy
Claudia Mosca
Affiliation:
Department of Biology, University of Rome Tor Vergata, Rome, Italy
Claudia Fagliarone
Affiliation:
Department of Biology, University of Rome Tor Vergata, Rome, Italy
Alessandro Napoli
Affiliation:
Department of Biology, University of Rome Tor Vergata, Rome, Italy
Cyprien Verseux
Affiliation:
University of Bremen, Center of Applied Space Technology and Microgravity, Bremen, Germany
Mickael Baqué
Affiliation:
German Aerospace Center, Institute of Planetary Research, Management and Infrastructure, Astrobiological Laboratories, Berlin, Germany
Jean-Pierre de Vera
Affiliation:
German Aerospace Center, Institute of Planetary Research, Management and Infrastructure, Astrobiological Laboratories, Berlin, Germany
Corresponding
E-mail address:

Abstract

By investigating the survival and the biomarker detectability of a rock-inhabiting cyanobacterium, Chroococcidiopsis sp. CCMEE 029, the BIOMEX space experiment might contribute to a future exploitation of the Moon as a test-bed for key astrobiology tasks such as the testing of life-detection technologies and the study of life in space. Post-flight analyses demonstrated that the mixing of dried cells with sandstone and a lunar regolith simulant provided protection against space UV radiation. During the space exposure, dried cells not mixed with minerals were killed by 2.05 × 102 kJ m−2 of UV radiation, while cells mixed with sandstone or lunar regolith survived 1.59 × 102 and 1.79 × 102 kJ m−2, respectively. No differences in survival occurred among cells mixed and not mixed with minerals and exposed to space conditions in the dark; this finding suggests that space vacuum and 0.5 Gy of ionizing radiation did not impair the cells’ presence in space. The genomic DNA of dead cells was severely damaged but still detectable with PCR amplification of a short target, thus suggesting that short sequences should be targeted in a PCR-based approach when searching for traces of life. The enhanced stability of genomic DNA of dried cells mixed with minerals and exposed to space indicates that DNA might still be detectable after prolonged periods, possibly up to millions of years in microbes shielded by minerals. Overall, the BIOMEX results contribute to future experiments regarding the exposure of cells and their biomarkers to deep space conditions in order to further test the lithopanspermia hypothesis, the biomarker stability and the microbial endurance, with implications for planetary protection and to determine if the Moon has been contaminated during past human missions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below.

References

Baqué, M, Verseux, C, Rabbow, E, de Vera, J-P and Billi, D (2014) Detection of macromolecules in desert cyanobacteria mixed with a lunar mineral analogue after space simulations. Origins of Life and Evolution of Biospheres 44, 209222.CrossRefGoogle ScholarPubMed
Baqué, M, Hanke, F, Böttger, U, Leya, T, Moeller, R and de Vera, J-P (2018) Protection of cyanobacterial carotenoids’ Raman signatures by Martian mineral analogues after high-dose gamma irradiation. Journal of Raman Spectroscopy 49, 16171627.CrossRefGoogle Scholar
Bernstein, M (2006) Prebiotic materials from on and off the early Earth. Philosophical Transactions of The Royal Society B: Biological Sciences 361, 16891700.CrossRefGoogle ScholarPubMed
Billi, D (2009) Subcellular integrities in Chroococcidiopsis sp. CCMEE 029 survivors after prolonged desiccation revealed by molecular probes and genome stability assays. Extremophiles 13, 4957.CrossRefGoogle ScholarPubMed
Billi, D (2010) Genetic tools for desiccation-, radiation-tolerant cyanobacteria of the genus Chroococcidiopsis. In Méndez-Vilas, A (ed.), Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. Badajoz, Spain: Formatex Research Center, pp. 15171521.Google Scholar
Billi, D (2012) Plasmid stability in dried cells of the desert cyanobacterium Chroococcidiopsis and its potential for GFP imaging of survivors on Earth and in space. Origins of Life and Evolution of Biospheres 42, 235245CrossRefGoogle ScholarPubMed
Billi, D (2018) Desert cyanobacteria under space and planetary simulations: a tool for searching for life beyond Earth and supporting human space exploration. International Journal of Astrobiology 17.Google Scholar
Billi, D, Viaggiu, E, Cockell, CS, Rabbow, E, Horneck, G and Onofri, S (2011) Damage escape and repair in dried Chroococcidiopsis spp. from hot and cold deserts exposed to simulated space and Martian conditions. Astrobiology 11, 6573.CrossRefGoogle ScholarPubMed
Billi, D, Baqué, M, Verseux, C, Rothschild, LJ and de Vera., J-P (2017) Desert cyanobacteria – potential for space and Earth applications. In Stan-Lotter, H and Fendrihan, S (eds), Adaption of Microbial Life to Environmental Extremes. Novel Research Results and Application, 2nd edn edn. Cham, Switzerland: Springer International Publishing, pp. 133146.CrossRefGoogle Scholar
Billi, D, Verseux, C, Fagliarone, C, Napoli, A, Baqué, M and de Vera, J-P (2019) A desert cyanobacterium under simulated Mars-like conditions in low Earth orbit: implications for the habitability of Mars. Astrobiology 19, 158169.CrossRefGoogle ScholarPubMed
Carpenter, JD, Fisackerly, R, De Rosa, D and Houdou, B (2012) Scientific preparations for lunar exploration with the European Lunar lander. Planetary and Space Science 74, 208223.CrossRefGoogle Scholar
Carr, CE, Rowedder, H, Vafadari, C, Lui, CS, Cascio, E, Zuber, MT and Ruvkun, G (2013) Radiation resistance of biological reagents for in situ life detection. Astrobiology 13, 6878.CrossRefGoogle ScholarPubMed
Cockell, CS (2008) The interplanetary exchange of photosynthesis. Origins of Life and Evolution of Biospheres 38, 87104.CrossRefGoogle ScholarPubMed
Cockell, CS (2010) Astrobiology – what can we do on the Moon?. Earth, Moon, and Planets 107, 310.CrossRefGoogle Scholar
Cockell, CS, Brack, A, Wynn-Williams, DD, Baglioni, P, Brandstätter, F, Demets, R, Edwards, HG, Gronstal, AL, Kurat, G, Lee, P, Osinski, GR, Pearce, DA, Pillinger, JM, Roten, CA and Sancisi-Frey, S (2007) Interplanetary transfer of photosynthesis: an experimental demonstration of a selective dispersal filter in planetary island biogeography. Astrobiology 7, 19.CrossRefGoogle ScholarPubMed
Crawford, IA, Anand, M, Cockell, CS, Falcke, HDE, Green, DA, Jaumann, R and Wieczorek, MA (2012) Back to the Moon: the scientific rationale for resuming lunar surface exploration. Planetary and Space Science 64, 314.CrossRefGoogle Scholar
Dachev, TP, Bankov, NG, Tomov, BT, Matviichuk, YN, Dimitrov, PG, Häder, D-P and Horneck, G (2017) Overview of the ISS radiation environment observed during the ESA EXPOSE-R2 mission in 2014–2016. Space Weather 15, 2016SW001580.CrossRefGoogle Scholar
de Vera, J-P and The Life Detection Group of BIOMEX/BioSigN (2019 a) A systematic way to life detection – combining field, lab and space research in low Earth orbit. In Cavalazzi, B and Westal, F (eds), Biosignatures for Astrobiology. Cham, Switzerland: Springer International Publishing, pp. 111122.CrossRefGoogle Scholar
de Vera, J-P, Boettger, U, de la Torre, R, Sanchez, FJ, Grunow, D, Schmitz, N, Lange, C, Hübers, H-W, Billi, D, Baqué, M, Rettberg, P, Rabbow, E, Reitz, G, Berger, T, Moeller, 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 and Spohn, T (2012) Supporting Mars exploration: BIOMEX in Low Earth Orbit and further astrobiological studies on the Moon using Raman and PanCam technology. Planetary and Space Science 74, 103110.CrossRefGoogle Scholar
de Vera, J-P, Alawi, M, Backhaus, T, Baqué, M, Billi, D, Böttger, U, Berger, T, Bohmeier, M, Cockell, CS, Demets, R, de la Torre Noetzel, R, Edwards, H, Elsaesser, A, Fagliarone, C, Fiedler, A, Foing, B, Foucher, F, Fritz, J, Hanke, F, Herzog, T, Horneck, G, Hübers, H-W, Huwe, B, Joshi, J, Kozyrovska, N, Kruchten, M, Lasch, P, Lee, N, Leuko, S, Leya, T, Lorek, A, Martínez-Frías, J, Meessen, J, Moritz, S, Moeller, R, Olsson-Francis, K, Onofri, S, Ott, S, Pacelli, C, Podolich, O, Rabbow, E, Reitz, G, Rettberg, P, Reva, O, Rothschild, L., Garcia Sancho, L., Schulze-Makuch, D., Selbmann, L., Serrano, P, Szewzyk, U, Verseux, C, Wadsworth, J, Wagner, D, Westall, F, Wolter, D and Zucconi, L (2019 b) Limits of life and the habitability of Mars: the ESA space experiment BIOMEX on the ISS. Astrobiology 19, 145157.CrossRefGoogle ScholarPubMed
Fagliarone, C, Mosca, C, Ubaldi, I, Verseux, C, Baqué, M, Wilmotte, A and Billi, D (2017) Avoidance of protein oxidation correlates with the desiccation and radiation resistance of hot and cold desert strains of the cyanobacterium Chroococcidiopsis. Extremophiles 21, 981991.CrossRefGoogle ScholarPubMed
Ferrari, F and Szuszkiewicz, E (2009) Cosmic rays: a review for astrobiologists. Astrobiology 9, 413436.CrossRefGoogle ScholarPubMed
Fox, S and Strasdeit, H (2017) Inhabited or uninhabited? Pitfalls in the interpretation of possible chemical signatures of extraterrestrial life. Frontiers in Microbiology 8, 1622.CrossRefGoogle ScholarPubMed
Gronstal, A, Cockell, CS, Perino, MA, Bittner, T, Clacey, E, Clark, O, Ingold, O, Alves de Oliveira, C and Wathiong, S (2007) Lunar astrobiology: a review and suggested laboratory equipment. Astrobiology 7, 767782.CrossRefGoogle ScholarPubMed
Horneck, G, Bücker, H and Reitz, G (1994) Long-term survival of bacterial spores in space. Advances in Space Research 14, 4145.CrossRefGoogle ScholarPubMed
Horneck, G, Rettberg, P, Reitz, G, Wehner, J, Eschweiler, U, Strauch, K, Panitz, C, Starke, V and Baumstark-Khan, C (2001) Protection of bacterial spores in space, a contribution to the discussion on Panspermia. Origins of Life and Evolution of Biospheres 31, 527547.CrossRefGoogle ScholarPubMed
Horneck, G, Stöffler, D, Ott, S, Hornemann, U, Cockell, CS, Möller, R, Meyer, C, de Vera, J-P, Fritz, J, Schade, S and Artemieva, N (2008) Microbial rock inhabitants survive hypervelocity impacts on Mars-like host planets: first phase of lithopanspermia experimentally tested. Astrobiology 8, 1744.CrossRefGoogle ScholarPubMed
Horneck, G, Klaus, DM and Mancinelli, RL (2010) Space microbiology. Microbiology and Molecular Biology Reviews 74, 121156.CrossRefGoogle ScholarPubMed
Johnson, SS, Anslyn, EV, Graham, HV, Mahaffy, PR and Ellington, AD (2018) Fingerprinting non-terran biosignatures. Astrobiology 18, 915922.CrossRefGoogle ScholarPubMed
Kitadai, N and Maruyama, S (2018) Origins of building blocks of life: a review. Geoscience Frontiers 9, 11171153.CrossRefGoogle Scholar
Koeberl, C (2003) The late heavy bombardment in the inner Solar System: Is there any connection to Kuiper Belt Objects? Earth, Moon, and Planets 92, 7987.CrossRefGoogle Scholar
Kumar, A, Tyagi, MB and Jha, PN (2004) Evidences showing ultraviolet-B radiation-induced damage of DNA in cyanobacteria and its detection by PCR assay. Biochemical and Biophysical Research Communications 318, 10251030.CrossRefGoogle ScholarPubMed
Loman, NJ and Watson, M (2015) Successful test launch for nanopore sequencing. Nature Methods 12, 303304.CrossRefGoogle ScholarPubMed
Mileikowsky, C, Cucinotta, FA, Wilson, JW, Gladman, B, Horneck, G, Lindegren, L, Melosh, J, Rickman, H, Valtonen, M and Zheng, JQ (2000) Natural transfer of viable microbes in space. Icarus 145, 391427.CrossRefGoogle ScholarPubMed
Needham, DH and Kring, DA (2017) Lunar volcanism produced a transient atmosphere around the ancient Moon. Earth and Planetary Science Letters 478, 175178.CrossRefGoogle Scholar
Nicholson, WL (2009) Ancient micronauts: interplanetary transport of microbes by cosmic impacts. Trends in Microbiology 17, 243250.CrossRefGoogle ScholarPubMed
Nicholson, WL, Munakata, N, Horneck, G, Melosh, HJ and Setlow, P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiology and Molecular Biology Reviews 64, 548572.CrossRefGoogle ScholarPubMed
Nicholson, WL, Schuerger, AC 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. Mutation Research 571, 249264.CrossRefGoogle ScholarPubMed
Puente-Sánchez, F, Arce-Rodríguez, A, Oggerin, M, García-Villadangos, M, Moreno-Paz, M, Blanco, Y, Rodríguez, N, Bird, L, Lincoln, SA, Tornos, F, Prieto-Ballesteros, O, Freeman, KH, Pieper, DH, Timmis, KN, Amils, R and Parro, V (2018) Viable cyanobacteria in the deep continental subsurface. Proceedings of the National Academy of Sciences of the USA 115, 1070210707.CrossRefGoogle Scholar
Rabbow, E, Parpart, A and Reitz, G (2016) The Planetary and space simulation facilities at DLR Cologne. Microgravity Science and Technology 28, 215229.CrossRefGoogle Scholar
Rabbow, E, Rettberg, P, Parpart, A, Panitz, C, Schulte, W, Molter, F, Jaramillo, E, Demets, R, Weiß, P and Willnecker, R (2017) EXPOSE-R2: the astrobiological ESA mission on board of the International Space Station. Frontiers in Microbiology 8, 1533.CrossRefGoogle ScholarPubMed
Reitz, G, Berger, T and Matthiae, D (2012) Radiation exposure in the Moon environment. Planetary and Space Science 74, 7883.CrossRefGoogle Scholar
Rippka, R, Deruelles, J, Waterbury, JB, Herdman, M and Stanier, RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111, 161.Google Scholar
Rudi, K, Hagen, I, Johnsrud, BC, Skjefstad, G and Tryland, I (2010) Different length (DL) qPCR for quantification of cell killing by UV-induced DNA damage. International Journal of Environmental Research and Public Health 7, 33763381.CrossRefGoogle ScholarPubMed
Schuerger, AC, Moores, JE, Smith, DJ and Reitz, G (2019) A lunar microbial survival model for predicting the forward contamination of the Moon. Astrobiology 19, 730756.CrossRefGoogle Scholar
Schulze-Makuch, D and Crawford, IA (2018) Was there an early habitability window for Earth's Moon? Astrobiology 18, 985988.CrossRefGoogle ScholarPubMed
Shirkey, B, McMaster, NJ, Smith, SC, Wright, DJ, Rodriguez, H, Jaruga, P, Birincioglu, M, Helm, RF and Potts, M (2003) Genomic DNA of Nostoc commune (Cyanobacteria) becomes covalently modified during long-term (decades) desiccation but is protected from oxidative damage and degradation. Nucleic Acids Research 31, 29953005.CrossRefGoogle ScholarPubMed
Verseux, C, Baqué, M, Cifariello, R, Fagliarone, C, Raguse, M, Moeller, R and Billi, D (2017) Evaluation of the resistance of Chroococcidiopsis spp. to sparsely and densely ionizing irradiation. Astrobiology 17, 118125.CrossRefGoogle ScholarPubMed
2
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Exposure to low Earth orbit of an extreme-tolerant cyanobacterium as a contribution to lunar astrobiology activities
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Exposure to low Earth orbit of an extreme-tolerant cyanobacterium as a contribution to lunar astrobiology activities
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Exposure to low Earth orbit of an extreme-tolerant cyanobacterium as a contribution to lunar astrobiology activities
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *