Exposure to low Earth orbit of an extreme-tolerant cyanobacterium as a contribution to lunar astrobiology activities
Abstract
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.
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The UV-exposed, non-protected by regolith sample of Chroococcidiopsis sp. CCMEE 029 did not demonstrate viability.
“The UV-exposed, non-protected by regolith sample of Chroococcidiopsis sp. CCMEE 029 did not demonstrate viability [111].”
After exposure to 0.5 Gy IR, vacuum, and in some cases UV, non-UV exposed and Lunar/Martian regolith analog samples of Chroococcidiopsis sp. CCMEE 029 proved viable after 672 of exposure to space in LEO.
“After exposure to 0.5 Gy of IR, as well as the vacuum of space and (in some cases) UV radiation, the samples were inoculated into growth medium for viability assessment. The non-UV exposed, as well as the Lunar and Martian regolith analog samples of Chroococcidiopsis sp. CCMEE 029 proved to be viable after 672 of exposure to space in LEO.”
Cites
Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria
Rippka, R., Stanier, R. Y., Deruelles, J., Herdman, M., & Waterbury, J. B. (1979) · Microbiology · doi:10.1099/00221287-111-1-1 · Cited by 7,606 · see citing works
Resistance ofBacillusEndospores to Extreme Terrestrial and Extraterrestrial Environments
Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., & Setlow, P. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.3.548-572.2000 · Cited by 2,041 · see citing works
Horneck, G., Klaus, D. M., & Mancinelli, R. L. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00016-09 · Cited by 619 · see citing works
Origins of building blocks of life: A review
Kitadai, N., & Maruyama, S. (2018) · Geoscience Frontiers · doi:10.1016/j.gsf.2017.07.007 · Cited by 464 · see citing works
Natural Transfer of Viable Microbes in Space 1. From Mars to Earth and Earth to Mars
Mileikowsky, C. (2000) · Icarus · doi:10.1006/icar.1999.6317 · Cited by 370 · see citing works
Long-Term Survival of Bacterial Spores in Space
Horneck, G., Bücker, H., & Reitz, G. (1994) · Advances in Space Research · doi:10.1016/0273-1177(94)90448-0 · Cited by 266 · see citing works
Protection of Bacterial Spores in Space, a Contribution to the Discussion on Panspermia
Horneck, G., Rettberg, P., Reitz, G., Wehner, J., Eschweiler, U., Strauch, K., Panitz, C., Starke, V., & Baumstark‐Khan, C. (2001) · Origins of Life and Evolution of Biospheres · doi:10.1023/a:1012746130771 · Cited by 201 · see citing works
Nicholson, W., Schuerger, A., & Setlow, P. (2005) · Mutation research · doi:10.1016/j.mrfmmm.2004.10.012 · Cited by 187 · see citing works
Back to the Moon: The scientific rationale for resuming lunar surface exploration
Crawford, I., Anand, M., Cockell, C. S., Falcke, H. D., Green, D. A., Jaumann, R., & Wieczorek, M. A. (2012) · Planetary and Space Science · doi:10.1016/j.pss.2012.06.002 · Cited by 181 · see citing works
Horneck, G., Stöffler, D., Ott, S., HORNEMANN, U., Cockell, C. S., Moeller, R., Meyer, C., Vera, J.-P. P. D., Fritz, J., Schade, S., et al. (2008) · Astrobiology · doi:10.1089/ast.2007.0134 · Cited by 174 · see citing works
Viable cyanobacteria in the deep continental subsurface
Puente‐Sánchez, F., Arce‐Rodríguez, A., Oggerin, M., García‐Villadangos, M., Moreno‐Paz, M., Blanco, Y., Rodríguez, N., Bird, L. R., Lincoln, S. A., Tornos, F., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1808176115 · Cited by 169 · see citing works
Limits of Life and the Habitability of Mars: The ESA Space Experiment BIOMEX on the ISS
Vera, J.-P. P. D., Alawi, M., Backhaus, T., Baqué, M., Billi, D., Böttger, U., Berger, T., Bohmeier, M., Cockell, C. S., Demets, R., et al. (2019) · Astrobiology · doi:10.1089/ast.2018.1897 · Cited by 162 · see citing works
Self-citationLunar volcanism produced a transient atmosphere around the ancient Moon
Needham, D. H., & KRING, D. A. (2017) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2017.09.002 · Cited by 147 · see citing works
Ancient micronauts: interplanetary transport of microbes by cosmic impacts
Nicholson, W. L. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.03.004 · Cited by 140 · see citing works
Successful test launch for nanopore sequencing
Loman, N. J., & Watson, M. (2015) · Nature Methods · doi:10.1038/nmeth.3327 · Cited by 131 · see citing works
Shirkey, B. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg404 · Cited by 114 · see citing works
EXPOSE-R2: The Astrobiological ESA Mission on Board of the International Space Station
Rabbow, E., Rettberg, P., Parpart, A., Panitz, C., Schulte, W., Molter, F., Jaramillo, E., Demets, R., Weiß, P., & Willnecker, R. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01533 · Cited by 100 · see citing works
Radiation exposure in the moon environment
Reitz, G., Berger, T., & Matthiae, D. (2012) · Planetary and Space Science · doi:10.1016/j.pss.2012.07.014 · Cited by 94 · see citing works
Billi, D. (2008) · Extremophiles · doi:10.1007/s00792-008-0196-0 · Cited by 91 · see citing works
Self-citationVera, J.-P. P. D., Boettger, U., Noetzel, R. D. L. T., Sánchez, F. J., Grunow, D., Schmitz, N., Lange, C., Hübers, H., Billi, D., Baqué, M., et al. (2012) · Planetary and Space Science · doi:10.1016/j.pss.2012.06.010 · Cited by 81 · see citing works
Self-citationOverview of the ISS Radiation Environment Observed during the ESA EXPOSE‐R2 Mission in 2014–2016
Dachev, T. P., Bankov, N. G., Tomov, B. T., et al. (2017) · Space Weather · doi:10.1002/2016sw001580 · Cited by 74 · see citing works
Kumar, A., Tyagi, M. B., & Jha, P. N. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.04.129 · Cited by 70 · see citing works
Cockell, C. S., Brack, A., Wynn-Williams, D. D., Baglioni, P., Brandstätter, F., Demets, R., Edwards, H. G. M., Gronstal, A., Kurat, G., Lee, P., et al. (2007) · Astrobiology · doi:10.1089/ast.2006.0038 · Cited by 68 · see citing works
Fingerprinting Non-Terran Biosignatures
Johnson, S. S., Anslyn, E. V., Graham, H. V., Mahaffy, P. R., & Ellington, A. D. (2018) · Astrobiology · doi:10.1089/ast.2017.1712 · Cited by 67 · see citing works
Billi, D., Viaggiu, E., Cockell, C. S., Rabbow, E., Horneck, G., & Onofri, S. (2011) · Astrobiology · doi:10.1089/ast.2009.0430 · Cited by 65 · see citing works
Self-citationBilli, D., Verseux, C., Fagliarone, C., Napoli, A., Baqué, M., & Vera, J.-P. P. D. (2019) · Astrobiology · doi:10.1089/ast.2017.1807 · Cited by 65 · see citing works
Self-citationPrebiotic materials from on and off the early Earth
Bernstein, M. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1913 · Cited by 64 · see citing works
Cosmic Rays: A Review for Astrobiologists
Ferrari, F., & Szuszkiewicz, E. (2009) · Astrobiology · doi:10.1089/ast.2007.0205 · Cited by 58 · see citing works
Fagliarone, C., Mosca, C., Ubaldi, I., Verseux, C., Baqué, M., Wilmotte, A., & Billi, D. (2017) · Extremophiles · doi:10.1007/s00792-017-0957-8 · Cited by 54 · see citing works
Self-citationThe Interplanetary Exchange of Photosynthesis
Cockell, C. S. (2007) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-007-9112-3 · Cited by 52 · see citing works
Verseux, C., Baqué, M., Cifariello, R., Fagliarone, C., Raguse, M., Moeller, R., & Billi, D. (2017) · Astrobiology · doi:10.1089/ast.2015.1450 · Cited by 52 · see citing works
Self-citationScientific preparations for lunar exploration with the European Lunar Lander
Carpenter, J. D., Fisackerly, R., Rosa, D. D., & Houdou, B. (2012) · Planetary and Space Science · doi:10.1016/j.pss.2012.07.024 · Cited by 47 · see citing works
Baqué, M., Hanke, F., Böttger, U., Leya, T., Moeller, R., & Vera, J.-P. P. D. (2018) · Journal of Raman Spectroscopy · doi:10.1002/jrs.5449 · Cited by 44 · see citing works
Self-citationBilli, D. (2018) · International Journal of Astrobiology · doi:10.1017/s147355041800037x · Cited by 40 · see citing works
Self-citationAstrobiology—What Can We Do on the Moon?
Cockell, C. S. (2010) · Earth Moon and Planets · doi:10.1007/s11038-010-9363-2 · Cited by 35 · see citing works
Koeberl, C. (2003) · Earth Moon and Planets · doi:10.1023/b:moon.0000031927.85937.9e · Cited by 32 · see citing works
Different Length (DL) qPCR for Quantification of Cell Killing by UV-induced DNA Damage
Rudi, K., Hagen, I., Johnsrud, B. C., et al. (2010) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph7093376 · Cited by 28 · see citing works
A Lunar Microbial Survival Model for Predicting the Forward Contamination of the Moon
Schuerger, A. C., Moores, J. E., Smith, D. J., & Reitz, G. (2019) · Astrobiology · doi:10.1089/ast.2018.1952 · Cited by 27 · see citing works
The Planetary and Space Simulation Facilities at DLR Cologne
Rabbow, E., Parpart, A., & Reitz, G. (2015) · Microgravity Science and Technology · doi:10.1007/s12217-015-9448-7 · Cited by 26 · see citing works
Koeberl, C. (2004) · Springer eBooks · doi:10.1007/978-94-017-3321-2_7 · Cited by 26 · see citing works
Was There an Early Habitability Window for Earth's Moon?
Schulze‐Makuch, D., & Crawford, I. (2018) · Astrobiology · doi:10.1089/ast.2018.1844 · Cited by 25 · see citing works
Lunar Astrobiology: A Review and Suggested Laboratory Equipment
Gronstal, A., Cockell, C. S., Perino, M. A., Bittner, T., Clacey, E., Clark, O., Ingold, O., de Oliveira, C. A., & Wathiong, S. (2007) · Astrobiology · doi:10.1089/ast.2006.0082 · Cited by 24 · see citing works
Desert Cyanobacteria: Potential for Space and Earth Applications
Billi, D., Baqué, M., Verseux, C., Rothschild, L. J., & Vera, J.-P. P. D. (2017) · Springer eBooks · doi:10.1007/978-3-319-48327-6_6 · Cited by 21 · see citing works
Self-citationRadiation Resistance of Biological Reagents for In Situ Life Detection
Carr, C. E., Rowedder, H., Vafadari, C., Lui, C. S., Cascio, E., Zuber, M. T., & Ruvkun, G. (2013) · Astrobiology · doi:10.1089/ast.2012.0869 · Cited by 20 · see citing works
Baqué, M., Verseux, C., Rabbow, E., Vera, J.-P. P. D., & Billi, D. (2014) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-014-9367-4 · Cited by 19 · see citing works
Self-citationBilli, D. (2012) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-012-9277-2 · Cited by 18 · see citing works
Self-citationFox, S., & Strasdeit, H. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01622 · Cited by 18 · see citing works
A Systematic Way to Life Detection: Combining Field, Lab and Space Research in Low Earth Orbit
The Life Detection Group of BIOMEX/BIOSIGN, & de Vera, J.-P. (2018) · Advances in astrobiology and biogeophysics · doi:10.1007/978-3-319-96175-0_5 · Cited by 10 · see citing works
Genetic tools for desiccation- and radiation-tolerant cyanobacteria of the genus Chroococcidiopsis
Billi, D. (2010) · Cited by 5 · see citing works
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Keller, R. J., Porter, W., Goli, K., Rosenthal, R., Butler, N., & Jones, J. A. (2021) · Life · doi:10.3390/life11080844 · Cited by 23 · see citing works
“CCMEE 029 did not demonstrate viability [111].”
- Authors
- Billi, D., Mosca, C., Fagliarone, C., Napoli, A., Verseux, C., Baqué, M., & de Vera, J.-P.
- Affiliations
- University of Rome Tor Vergata (IT)
- University of Bremen (DE)
- Corresponding author
- Billi, Daniela
- Venue
- International Journal of Astrobiology
- Publisher
- Cambridge University Press (CUP)
- Published
- 2019-07-18
- Volume
- 19
- Issue
- 1
- Pages
- 53-60
- ISSN
- 1473-5504 (ISSN-L)
- 1475-3006
- OpenAlex
- W2963631456
- Cited by
- 6
- References
- 49
- Citations by year
- 2026: 1 · 2025: 1 · 2022: 1 · 2021: 1 · 2020: 2
- FWCI
- 0.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Journal of Astrobiology (publishedVersion)
- elib (German Aerospace Center) (acceptedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Space Science and Extraterrestrial Life
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Planetary Science and Exploration
- Health Sciences › Medicine › Physiology › Spaceflight effects on biology
- Keywords
- Chroococcidiopsis, space exposure, low Earth orbit, lunar regolith simulant, sandstone, ultraviolet radiation, microbial survival, biomarker detection, life detection, lithopanspermia, planetary protection, ionizing radiation
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