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Desert cyanobacteria under space and planetary simulations: a tool for searching for life beyond Earth and supporting human space exploration

Published online by Cambridge University Press:  12 September 2018

Daniela Billi Open the ORCID record for Daniela Billi [Opens in a new window]
Daniela Billi*
Affiliation:
Department of Biology, University of Rome “Tor Vergata”, Via della Ricerca Scientifica, s.n.c 00133 Rome, Italy
*
Author for correspondence: Daniela Billi, E-mail: billi@uniroma2.it
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Abstract

The astonishing capability of life to adapt to extreme conditions has provided a new perspective on what ‘habitable’ means. On Earth extremophiles thrive in hostile habitats, such as hot and cold deserts or Antarctic sub-glacial lakes considered as Earth analogues of Mars and icy moons of Jupiter and Saturn. Recently desert cyanobacteria were exposed to ground-based simulations of space and Martian conditions and to real space and Martian conditions simulated in low Earth orbit using facilities attached outside the International Space Station. When exposure to such conditions does not exceed repair capabilities, more data are available regarding the physico-chemical constraints that life can withstand. When the accumulated damage exceeds the survival potential, the persistence of biomarkers contributes to the search for life elsewhere. Knowledge concerning the endurance of desert cyanobacteria under space and Martian conditions contributes to the development of life support systems.

Keywords

Chroococcidiopsisdesiccation tolerancedesert cyanobacterialife supportlow Earth orbitMars-like conditionsradiation tolerancespace exposurespace synthetic biology
Type
Review Article
Information
International Journal of Astrobiology , Volume 18 , Issue 5 , October 2019 , pp. 483 - 489
Copyright
Copyright © Cambridge University Press 2018 

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References

Baqué, M, Viaggiu, E, Scalzi, G and Billi, D (2013 a) Endurance of the endolithic desert cyanobacterium Chroococcidiopsis under UVC radiation. Extremophiles 17, 161–169.Google Scholar
Baqué, M, de Vera, J-P, Rettberg, P and Billi, D (2013 b) 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 Astronautica 91, 180–186.Google Scholar
Baqué, M, Scalzi, G, Rabbow, E, Rettberg, P and Billi, D (2013 c) Biofilm and planktonic lifestyles differently support the resistance of the desert cyanobacterium Chroococcidiopsis under space and Martian simulations. Origins of Life and Evolution of the Biosphere 3, 377–389.Google Scholar
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, 209–222.Google Scholar
Baqué, M, Verseux, C, Böttger, U, Rabbow, E, de Vera, J-P and Billi, D (2016) Preservation of biomarkers from cyanobacteria mixed with Mars-like regolith under simulated Martian atmosphere and UV flux. Origin Life and Evolution of Biospheres 46, 289–310.Google Scholar
Billi, D (2009) Subcellular integrities in Chroococcidiopsis sp. CCMEE 029 survivors after prolonged desiccation revealed by molecular probes and genome stability assays. Extremophiles 13, 49–57.Google Scholar
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. Vol II. Spain: Format Research Center, pp. 1517–1521.Google Scholar
Billi, D (2012 a) Anhydrobiotic rock-inhabiting cyanobacteria: potential for astrobiology and biotechnology. In Stan-Lotter, H and Fendrihan, S (ed.), Adaption of Microbial Life to Environmental Extremes. Novel Research Results and Application. Springer-Verlag Wien, pp. 119–132.Google Scholar
Billi, D (2012 b) 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, 235–245.Google Scholar
Billi, D, Friedmann, EI, Hofer, KG, Grilli Caiola, M and Ocampo-Friedmann, R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Applied and Environmental Microbiology 66, 1489–1492.Google Scholar
Billi, D, Friedmann, EI, Helm, RF and Potts, M (2001) Gene transfer to the desiccation-tolerant cyanobacterium Chroococcidiopsis. Journal of Bacteriology 183, 2298–2305.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, 65–73.Google Scholar
Billi, D, Baqué, M, Smith, DH and McKay, CP (2013) Cyanobacteria from extreme deserts to space. Advances in Microbiology 3, 80–86.Google Scholar
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. Springer International Publishing, pp. 133–146.Google Scholar
Bryce, CC, Horneck, G, Rabbow, E, Edwards, HGM and Cockell, CS (2015) Impact shocked rocks as protective habitats on an anoxic early Earth. International Journal of Astrobiology 14, 115–122.Google Scholar
Claudi, R, Erculiani, MS, Galletta, G, Billi, D, Pace, E, Schierano, D, Giro, E and D'Alessandro, M (2016) Simulating super Earth atmospheres in the laboratory. International Journal of Astrobiology 15, 35–44.Google Scholar
Cockell, CS, Schuerger, AC, Billi, D, Friedmann, EI and Panitz, C (2005) Effects of a Simulated Martian UV Flux on the cyanobacterium, Chroococcidiopsis sp. 029. Astrobiology 5, 127–140.Google 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, 1–9.Google Scholar
Cockell, CS, Rettberg, P, Rabbow, E and Olsson-Francis, K (2011) Exposure of phototrophs to 548 days in low Earth orbit: microbial selection pressures in outer space and on early Earth. The ISME Journal 5, 1671–1682.Google Scholar
Cockell, CS, Bush, T, Bryce, C, Direito, S, Fox-Powell, M, Harrison, JP, Lammer, H, Landenmark, H, Martin-Torres, J, Nicholson, N, Noack, L, O'Malley-James, J, Payler, SJ, Rushby, A, Samuels, T, Schwendner, P, Wadsworth, J and Zorzano, MP (2016) Habitability: a review. Astrobiology 16, 89–117.Google Scholar
Cottin, H, Kotler, JM, Bartik, K, Cleaves, HJ, Cockell, CS, de Vera, J-P, Ehrenfreund, P, Leuko, S, Ten Kate, IL, Martins, Z, Pascal, R, Quinn, R, Rettberg, P and Westall, F (2017 a) Astrobiology and the possibility of life on Earth and elsewhere…. Space Science Reviews 209, 1–42.Google Scholar
Cottin, H, Kotler, JM, Billi, D, Cockell, C, Demets, R, Ehrenfreund, P, Elsaesser, A, d'Hendecourt, L, van Loon, JJWA, Martins, Z, Onofri, S, Quinn, RC, Rabbow, E, Rettberg, P, Ricco, AJ, Slenzka, K, de la Torre, R, de Vera, J-P, Westall, F, Carrasco, N, Fresneau, A, Kawaguchi, Y, Kebukawa, Y, Nguyen, D, Poch, O, Saiagh, K, Stalport, F, Yamagishi, A, Yano, H and Klamm, BA (2017 b) Space as a tool for astrobiology: review and recommendations for experimentations in Earth orbit and beyond. Space Science Reviews 209, 83–181.Google 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, 1475–1489.Google Scholar
Deamer, D and Damer, B (2017) Can life begin on Enceladus? A perspective from hydrothermal chemistry. Astrobiology 17, 834–839.Google Scholar
de Vera, J-P, Boettger, U, de al Torre, R, Sanchez, FJ, Grunow, D, Schmitz, N, Lange, C, Hübers, H-W, Billi, D, Baque, 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 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, 103–110.Google Scholar
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. Extremophlies 21, 981–991.Google Scholar
Flemming, H-C, Wingender, J, Szewzyk, U, Steinberg, P, Rice, SA and Kjelleberg, S (2016) Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology 14, 563–575.Google Scholar
Friedmann, EI and Ocampo-Friedmann, R (1976) Endolithic blue-green-algae in dry valleys-primary producers in Antarctic desert ecosystem. Science 193, 1247–1249.Google Scholar
Friedmann, I, Lipkin, Y and Ocampo-Paus, R (1967) Desert algae of the Negev. Phycologia 6, 185–196.Google Scholar
Harrison, JP, Gheeraert, N, Tsigelnitskiy, D and Cockell, CS (2013) The limits for life under multiple extremes. Trends in Microbiology 21, 204–212.Google Scholar
Hassler, DM, Zeitlin, C, Wimmer-Schweingruber, RF, Ehresmann, B, Rafkin, S, Eigenbrode, JL, Brinza, DE, Weigle, G, Böttcher, S, Böhm, E, Burmeister, S, Guo, J, Köhler, J, Martin, C, Reitz, G, Cucinotta, FA, Kim, MH, Grinspoon, D, Bullock, MA, Posner, A, Gómez-Elvira, J, Vasavada, A, Grotzinger, JP and MSL Science Team (2013) The radiation environment on the surface of Mars measured on the Mars Science Laboratory's Curiosity rover. Science 343, 1244797.Google Scholar
Hecht, MH, Kounaves, SP, Quinn, RC, West, SJ, Young, SM, Ming, DW, Catling, DC, Clark, BC, Boynton, WV, Hoffman, J, Deflores, LP, Gospodinova, K, Kapit, J and Smith, PH (2009) Detection of perchlorate and the soluble chemistry of Martian soil at the Phoenix lander site. Science 325, 64–66.Google Scholar
Hendrickx, L, De Wever, H, Hermans, V, Mastroleo, F, Morin, N, Wilmotte, A, Janssen, P and Mergeay, M (2006) Microbial ecology of the closed artificial ecosystem MELiSSA (Micro-Ecological Life Support System Alternative): reinventing and compartmentalizing the Earth's food and oxygen regeneration system for long-haul space exploration missions. Research in Microbiology 157, 77–78.Google Scholar
Ho, MY, Shen, G, Canniffe, DP, Zhao, C and Bryant, DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353, aaf9178–1.Google Scholar
Horneck, G, Klaus, DM and Mancinelli, RL (2010) Space microbiology. Microbiology and Molecular Biology Reviews 74, 121–156.Google Scholar
Horneck, G, Walter, N, Westall, F, Grenfell, JL, Martin, WF, Gomez, F, Leuko, S, Lee, N, Onofri, S, Tsiganis, K, Saladino, R, Pilat-Lohinger, E, Palomba, E, Harrison, J, Rull, F, Muller, C, Strazzulla, G, Brucato, JR, Rettberg, P and Capria, MT (2016) Astromap European astrobiology roadmap. Astrobiology 16, 201–243.Google Scholar
Kaltenegger, L (2017) How to characterize habitable worlds and signs of life. Annual Review of Astronomy and Astrophysics 55, 433–485.Google Scholar
Khalil, AS and Collins, JJ (2010) Synthetic biology: applications come of age. Nature Reviews Genetics 11, 367–379.Google Scholar
Martins, Z, Cottin, H, Kotler, JM, Carrasco, N, Cockell, CS, de la Torre Noetzel, R, Demets, R, de Vera, J-P, d'Hendecourt, L, Ehrenfreund, P, Elsaesser, A, Foing, B, Onofri, S, Quinn, R, Rabbow, E, Rettberg, P, Ricco, AJ, Slenzka, K, Stalport, F, ten Kate, IL, van Loon, JJWA and Westall, F (2017) Earth as a tool for astrobiology – a European perspective. Space Science Reviews 209, 43–81.Google Scholar
Matsubara, T, Fujishima, K, Saltikov, CW, Nakamura, S and Rothschild, LJ (2017) Earth analogues for past and future life on Mars: isolation of perchlorate resistant halophiles from Big Soda Lake. International Journal of Astrobiology 16, 218–228.Google Scholar
Moeller, R, Raguse, M, Leuko, S, Berger, T, Hellweg, CE, Fujimori, A, Okayasu, R, Horneck, G and the STARLIFE Research Group (2017) STARLIFE – an international campaign to study the role of galactic cosmic radiation in astrobiological model systems. Astrobiology 17, 101–109.Google Scholar
Nicholson, WL (2009) Ancient micronauts: interplanetary transport of microbes by cosmic impacts. Trends in Microbiology 17, 243–250.Google Scholar
Olsson-Francis, K and Cockell, CS (2010) Use of cyanobacteria for in-situ resource use in space applications. Planetary and Space Science 58, 1279–1285.Google Scholar
Olsson-Francis, K, de la Torre, R, Towner, MC and Cockell, CS (2009) Survival of akinetes (resting-state cells of cyanobacteria) in low earth orbit and simulated extraterrestrial conditions. Origins of Life and Evolution of Biospheres 39, 565–576.Google Scholar
Panitz, C, Rettberg, P, Rabbow, E, Bauermeister, A, Barczyk, S, Billi, D, Cockell, CS, Flemming, H-C, Stan-Lotter, H and Venkateswaran, K (2012) The experiment BOSS on EXPOSE R-2, mission preparation tests for biofilm organisms surfing space. EPSC Abstracts Vol. 7 EPSC2012-447-1 2012 European Planetary Science Congress.Google Scholar
Pettinelli, E, Cosciotti, B, Di Paolo, F, Lauro, SE, Mattei, E, Orosei, R and Vannaroni, G (2015) Dielectric properties of Jovian satellite ice analogs for subsurface radar exploration: a review. Reviews of Geophysics 53, 593–641.Google Scholar
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.Google 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.Google Scholar
Rothschild, LJ (2016) Synthetic biology meets bioprinting: enabling technologies for humans on Mars (and Earth). Biochemical Society Transactions 44, 1158–1164.Google Scholar
Schwieterman, EW, Kiang, NY, Parenteau, MN, Harman, CE, DasSarma, S, Fisher, TM, Arney, GN, Hartnett, HE, Reinhard, CT, Olson, SL, Meadows, VS, Cockell, CS, Walker, SI, Grenfell, JL, Hegde, S, Rugheimer, S, Hu, R and Lyons, TW (2018) Exoplanet biosignatures: a review of remotely detectable signs of life. Astrobiology 18, 663–708.Google Scholar
Smith, HD, Baqué, M, Duncan, DA, McKay, CP and Billi, D (2014) Comparative analysis of cyanobacteria inhabiting rocks with different light transmittance in the Mojave Desert: a Mars terrestrial analogue. International Journal of Astrobiology 13, 271–277.Google Scholar
Verseux, C, Baqué, M, Lehto, K, de Vera, J-P, Rothschild, LJ and Billi, D (2016a) Sustainable life support on Mars – the potential roles of cyanobacteria. International Journal of Astrobiology 15, 65–92.Google Scholar
Verseux, C, Paulino-Lima, IG, Baqué, M, Billi, D and Rothschild, LJ (2016 b) Synthetic biology for space exploration: promises and societal implications. In Hagen, K, Engelhard, M and Toepfer, G (eds), Ambivalences of Creating Life. Societal and Philosophical Dimensions of Synthetic Biology. Series Ethics of Science and Technology Assessment. Berlin, Heidelberg: Springer-Verlag, pp. 73–100.Google Scholar
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, 118–125.Google Scholar
Westall, F, Loizeau, D, Foucher, F, Bost, N, Betrand, M, Vago, J and Kminek, G (2013) Habitability on Mars from a microbial point of view. Astrobiology 13, 887–897.Google Scholar