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Fungal biomarkers are detectable in Martian rock-analogues after space exposure: implications for the search of life on Mars

Published online by Cambridge University Press:  18 October 2021

Claudia Pacelli
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy Italian Space Agency, Scientific Research Unit, Via del Politecnico snc, 00133 Rome, Italy
Alessia Cassaro*
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
Mickael Baqué
Affiliation:
Planetary Laboratories Department, German Aerospace Center (DLR), Institute of Planetary Research, Ruthefordstraße 2, Berlin, Germany
Laura Selbmann
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy Italian Antarctic National Museum (MNA), Mycological Section, 16128 Genoa, Italy
Laura Zucconi
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
Alessandro Maturilli
Affiliation:
Planetary Laboratories Department, German Aerospace Center (DLR), Institute of Planetary Research, Ruthefordstraße 2, Berlin, Germany
Lorenzo Botta
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
Raffaele Saladino
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
Ute Böttger
Affiliation:
Department Terahertz and Laser Spectroscopy, German Aerospace Center (DLR) Berlin, Institute of Optical Sensor Systems, Rutherfordstr. 2, 12489 Berlin, Germany
René Demets
Affiliation:
European Space Agency, ESTEC, Keplerlaan 1, 2201AZ Noordwijk, The Netherlands
Elke Rabbow
Affiliation:
German Aerospace Center (DLR) Cologne, Institute of Aerospace Medicine, Radiation Biology, Linder Höhe, 51147 Cologne, Germany
Jean-Pierre P. de Vera
Affiliation:
MUSC, German Aerospace Center (DLR), Space Operations and Astronaut Training, Linder Höhe, Cologne-Porz, Germany
Silvano Onofri
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
*
Author for correspondence: Alessia Cassaro, E-mail: cassaro@unitus.it

Abstract

Mars is a primary target of astrobiological interest: its past environmental conditions may have been favourable to the emergence of a prebiotic chemistry and, potentially, biological activity. In situ exploration is currently underway at the Mars surface, and the subsurface (2 m depth) will be explored in the future ESA ExoMars mission. In this context, BIOlogy and Mars EXperiment was performed to evaluate the stability and detectability of organic biomarkers under space and Mars-like conditions. Our data suggested that some target molecules, namely melanin, azelaic acid and nucleic acids, can be detected even after 16 months exposure to Low Earth Orbit conditions by multidisciplinary approaches. We used the same techniques as onboard the ExoMars rover, as Raman and infrared spectroscopies and gas chromatograph-mass spectrometer, and polymerase chain reaction even if this is not planned for the imminent mission to Mars. These results should be taken into account for future Mars exploration.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

Authors have equally contributed to coordinate the research.

References

Baqué, M, Hanke, F, Böttger, U, Leya, T, Moeller, R and de Vera, JP (2018) Protection of cyanobacterial carotenoids’ Raman signatures by Martian mineral analogues after high-dose gamma irradiation. Journal of Raman Spectroscopy 49, 16171627.CrossRefGoogle Scholar
Baraldi, D (1973) Effect of gamma radiation on D-glucose present in apple juice. Journal of Food Science 38, 108111.CrossRefGoogle Scholar
Berger, T, Bilski, P, Hajek, M, Puchalska, M and Reitz, G (2013) The MATROSHKA experiment: results and comparison from extravehicular activity (MTR-1) and intravehicular activity (MTR-2A/2B) exposure. Journal of Radiation Research 180, 622637.CrossRefGoogle ScholarPubMed
Bibring, JP, Langevin, Y, Mustard, JF, Poulet, F, Arvidson, R, Gendrin, A and Berthe, M (2006) Global mineralogical and aqueous Mars history derived from OMEGA/Mars express data. Science (New York, N.Y.) 312, 400404.CrossRefGoogle ScholarPubMed
Biemann, K (2007) On the ability of the Viking gas chromatograph-mass spectrometer to detect organic matter. Proceedings of the National Academy of Sciences of the USA 104, 1031010313.CrossRefGoogle ScholarPubMed
Blois, MS (1965) Random polymers as a matrix for chemical evolution. In Fox, SW (Sep 03, 2013, Elseiver), The Origins of Pre-Biological Systems and of Their Molecular Matrices: Proceedings of a Conference, Wakulla Springs, Florida, 27–30 October 1963, pp. 1938.CrossRefGoogle Scholar
Böttger, U, de Vera, JP, Fritz, J, Weber, I, Hübers, HW and Schulze-Makuch, D (2012) Optimizing the detection of carotene in cyanobacteria in a Martian regolith analogue with a Raman spectrometer for the ExoMars mission. Planetary and Space Science 60, 356362.CrossRefGoogle Scholar
Capozzi, V, Perna, G, Gallone, A, Biagi, PF, Carmone, P, Fratello, A and Cicero, R (2005) Raman and optical spectroscopy of eumelanin films. Journal of Molecular Structure 744, 717721.CrossRefGoogle Scholar
Carbone, I and Kohn, LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91, 553556.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
Centeno, SA and Shamir, J (2008) Surface enhanced Raman scattering (SERS) and FTIR characterization of the sepia melanin pigment used in works of art. Journal of Molecular Structure 873, 149159.CrossRefGoogle Scholar
Chevrier, V and Mathé, PE (2007) Mineralogy and evolution of the surface of Mars: a review. Planetary and Space Science 55, 289314.CrossRefGoogle Scholar
Chevrier, V, Poulet, F and Bibring, JP (2007) Early geochemical environment of Mars as determined from thermodynamics of phyllosilicates. Nature 448, 6063.CrossRefGoogle Scholar
Cockell, CS (2014) Trajectories of Martian habitability. Astrobiology 14, 182203.CrossRefGoogle ScholarPubMed
Cubeta, MA, Echandi, E, Abernethy, T and Vilgalys, R (1991) Characterization of anastomosis groups of binucleate Rhizoctonia species using restriction analysis of an amplified ribosomal RNA gene. Phytopathology 81, 13951400.CrossRefGoogle Scholar
Culka, A, Jehlička, J, Ascaso, C, Artieda, O, Casero, CM and Wierzchos, J (2017) Raman microspectrometric study of pigments in melanized fungi from the hyperarid Atacama desert gypsum crust. Journal of Raman Spectroscopy 48, 14871493.CrossRefGoogle Scholar
Dartnell, LR, Desorgher, L, Ward, JM and Coates, AJ (2007) Modelling the surface and subsurface Martian radiation environment: implications for astrobiology. Geophysical Research Letters 34 (2). https://doi.org/10.1029/2006GL027494.CrossRefGoogle Scholar
Dartnell, LR, Page, K, Jorge-Villar, SE, Wright, G, Munshi, T, Scowen, IJ and Edwards, HG (2012 a) Destruction of Raman biosignatures by ionising radiation and the implications for life detection on Mars. Analytical and Bioanalytical Chemistry 403, 131144.CrossRefGoogle ScholarPubMed
Dartnell, LR, Desorgher, L, Ward, JM and Coates, AJ (2012 b) Martian sub-surface ionising radiation: biosignatures and geology. Biogeosciences (Online) 4, 545558.CrossRefGoogle Scholar
Deamer, DW and Pashley, RM (1989) Amphiphilic components of the Murchison carbonaceous chondrite: surface properties and membrane formation. Origins of Life and Evolution of the Biosphere: The Journal of the International Society for the Study of the Origin of Life 19, 2138.CrossRefGoogle ScholarPubMed
de Vera, J-PP, Boettger, U, de la Torre Noetzel, R, Sánchez, FJ, Grunow, D, Schmitz, N and Rettberg, P (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, 03110.CrossRefGoogle Scholar
de Vera, J-PP, Alawi, M, Backhaus, T, Baqué, M, Billi, D, Böttger, U and de la Torre Noetzel, R (2019) Limits of life and the habitability of Mars: the ESA space experiment BIOMEX on the ISS. Astrobiology 19, 145157.CrossRefGoogle ScholarPubMed
Dhole, PD, Khollam, YB, Gunjal, SD, Shelke, PN and Jadkar, SR (2016) Melanin thin films prepared by electrochemical deposition method and their characterizations. International Journal of Chemical and Physical Sciences 5, 110.Google Scholar
Dovbeshko, GI, Gridina, NY, Kruglova, EB and Pashchuk, OP (2000) FTIR spectroscopy studies of nucleic acid damage. Talanta 53, 233246.CrossRefGoogle ScholarPubMed
Edwards, HGM, Jehlička, J and Culka, A (2021) Portable Raman spectroscopy in field geology and astrobiology applications. Portable Spectroscopy and Spectrometry 1: Applications 2, 377400.CrossRefGoogle Scholar
Eisenman, HC and Casadevall, A (2012) Synthesis and assembly of fungal melanin. Applied Microbiology and Biotechnology 93, 931940.CrossRefGoogle ScholarPubMed
Fabian, H, Jackson, M, Murphy, L, Watson, PH, Fichtner, I and Mantsch, HHA (1995) Comparative infrared spectroscopic study of human breast tumors and breast tumor cell xenografts. Biospectroscopy 1, 3745.CrossRefGoogle Scholar
Ferrari, AC, Rodil, SE and Robertson, J (2003) Interpretation of infrared and Raman spectra of amorphous carbon nitrides. Physical Review B 67, 155306.CrossRefGoogle Scholar
Forfang, K, Zimmermann, B, Kosa, G, Kohler, A and Shapaval, V (2017) FTIR spectroscopy for evaluation and monitoring of lipid extraction efficiency for oleaginous fungi. PLoS ONE 12, 117.CrossRefGoogle ScholarPubMed
Friedmann, EI (1986) The Antarctic cold desert and the search for traces of life on Mars. Advances in Space Research 6, 265268.CrossRefGoogle ScholarPubMed
Galván, I, Jorge, A, Ito, K, Tabuchi, K, Solano, F and Wakamatsu, K (2013) Raman spectroscopy as a non-invasive technique for the quantification of melanins in feathers and hairs. Pigment Cell & Melanoma Research 26, 917923.CrossRefGoogle ScholarPubMed
Georgiou, CD and Deamer, DW (2014) Lipids as universal biomarkers of extraterrestrial life. Astrobiology 14, 541549.CrossRefGoogle ScholarPubMed
Glass, K, Ito, S, Wilby, PR, Sota, T, Nakamura, A, Bowers, CR and Wakamatsu, K (2012) Direct chemical evidence for eumelanin pigment from the Jurassic period. Proceedings of the National Academy of Sciences of the USA 109, 1021810223.CrossRefGoogle ScholarPubMed
Hallsworth, JE (2021) Mars’ surface is not universally biocidal. Environmental Microbiology, 23(7), 3345–3350. https://doi.org/10.1111/1462-2920.15494.CrossRefGoogle Scholar
Holland, PM, Chutjian, A, Darrach, MR and Orient, OJ (2003) Miniaturized GC/MS instrumentation for in situ measurements: micro gas chromatography coupled with miniature quadrupole array and Paul ion trap mass spectrometers. Proceedings of the SPIE 4878, First Jet Propulsion Laboratory In Situ Instruments Workshop, (25 July 2003). https://doi.org/10.1117/12.520539.CrossRefGoogle Scholar
Kminek, G, Conley, C, Allen, CC, Bartlett, DH, Beaty, DW, Benning, LG and Westall, F (2014) Report of the workshop for life detection in samples from Mars. Life Sciences in Space Research 2, 15.CrossRefGoogle Scholar
Korablev, OI, Dobrolensky, Y, Evdokimova, N, Fedorova, AA, Kuzmin, RO, Mantsevich, SN and Griffiths, A (2017) Infrared spectrometer for ExoMars: a mast-mounted instrument for the rover. Astrobiology 17, 542564.CrossRefGoogle ScholarPubMed
Leuko, S, Bohmeier, M, Hanke, F, Böettger, U, Rabbow, E, Parpart, A and de Vera, J-PP (2017) On the stability of deinoxanthin exposed to Mars conditions during a long-term space mission and implications for biomarker detection on other planets. Frontiers in Microbiology 8, 111.CrossRefGoogle ScholarPubMed
Maggiori, C, Stromberg, J, Blanco, Y, Goordial, J, Cloutis, E, García-Villadangos, M and Whyte, L (2020) The limits, capabilities, and potential for life detection with MinION sequencing in a paleochannel Mars analog. Astrobiology 20, 375393.CrossRefGoogle Scholar
Mahaffy, P (2008) Exploration of the habitability of Mars: development of analytical protocols for measurement of organic carbon on the 2009 Mars science laboratory. Space Science Reviews 135, 255268.CrossRefGoogle Scholar
McCollom, TM and Hynek, BM (2005) A volcanic environment for bedrock diagenesis at Meridiani Planum on Mars. Nature 438, 11291131.CrossRefGoogle ScholarPubMed
McMahon, S (2021) Astrobiology (overview). Oxford Research Encyclopedia of Planetary Science. Retrieved from https://oxfordre.com/planetaryscience/view/10.1093/acrefore/9780190647926.001.0001/acrefore-9780190647926-e-1 on 10/13/2021.Google Scholar
Morris, RV, Ruff, SW, Gellert, R, Ming, DW, Arvidson, RE, Clark, BC and Fleischer, I (2010) Identification of carbonate-rich outcrops on Mars by the spirit rover. Science (New York, N.Y.) 329, 421424.CrossRefGoogle ScholarPubMed
Movasaghi, Z, Rehman, S and Rehman, IU (2008) Fourier transform infrared (FTIR) spectroscopy of biological tissues. Applied Spectroscopy Reviews 43, 134179.CrossRefGoogle Scholar
Mustard, JF, Ehlmann, BL, Murchie, SL, Poulet, F, Mangold, N, Head, JW and Roach, LH (2009) Composition, morphology, and stratigraphy of Noachian crust around the Isidis basin. Journal of Geophysical Research 114, E00D12.CrossRefGoogle Scholar
Naraoka, H, Shimoyama, A and Harada, K (1999) Molecular distribution of monocarboxylic acids in Asuka carbonaceous chondrites from Antarctica. Origins of Life and Evolution of the Biosphere: The Journal of the International Society for the Study of the Origin of Life 29, 187201.CrossRefGoogle ScholarPubMed
Nazzaro-Porro, M (1987) Azelaic acid. JAAD 17, 10331041.CrossRefGoogle ScholarPubMed
Novotný, O, Cejpek, K and Velíšek, J (2008) Formation of carboxylic acids during degradation of monosaccharides. Czech Journal of Food Sciences 26, 117131.CrossRefGoogle Scholar
Onofri, S, de la Torre, R, de Vera, JP, Ott, S, Zucconi, L, Selbmann, L and Horneck, G (2012) Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12, 508516.CrossRefGoogle ScholarPubMed
Onofri, S, de Vera, JP, Zucconi, L, Selbmann, L, Scalzi, G, Venkateswaran, KJ and Horneck, G (2015) Survival of Antarctic cryptoendolithic fungi in simulated Martian conditions on board the International Space Station. Astrobiology 15, 10521059.CrossRefGoogle ScholarPubMed
Onofri, S, Selbmann, L, Pacelli, C, Zucconi, L, Rabbow, E and de Vera, JP (2019) Survival, DNA, and ultrastructural integrity of a cryptoendolithic Antarctic fungus in Mars and lunar rock analogs exposed outside the International Space Station. Astrobiology 19, 170182.CrossRefGoogle ScholarPubMed
Pacelli, C, Selbmann, L, Zucconi, L, De Vera, JP, Rabbow, E, Horneck, G and Onofri, S (2017) BIOMEX experiment: ultrastructural alterations, molecular damage and survival of the fungus Cryomyces antarcticus after the experiment verification tests. Origins of Life and Evolution of the Biosphere: The Journal of the International Society for the Study of the Origin of Life 47, 187202.CrossRefGoogle ScholarPubMed
Pacelli, C, Bryan, RA, Onofri, S, Selbmann, L, Zucconi, L, Shuryak, I and Dadachova, E (2018) The effect of protracted X-ray exposure on cell survival and metabolic activity of fast and slow growing fungi capable of melanogenesis. Environmental Microbiology Reports 10, 255263.CrossRefGoogle ScholarPubMed
Pacelli, C, Cassaro, A, Maturilli, A, Timperio, AM, Gevi, F, Cavalazzi, B and Onofri, S (2020) Multidisciplinary characterization of melanin pigments from the black fungus Cryomyces antarcticus. Applied Microbiology and Biotechnology, 104, 63856395.CrossRefGoogle ScholarPubMed
Parnell, J, Cullen, D, Sims, MR, Bowden, S, Cockell, CS, Court, R and Rohmer, M (2007) Searching for life on Mars: selection of molecular targets for ESA's Aurora ExoMars mission. Astrobiology 7, 578604.CrossRefGoogle ScholarPubMed
Pinkert, S and Zeuss, D (2018) Thermal biology: melanin-based energy harvesting across the tree of life. Current Biology 28, R887R889.CrossRefGoogle ScholarPubMed
Poulet, F, Bibring, JP, Mustard, JF, Gendrin, A, Mangold, N, Langevin, Y and Gomez, C (2005) Phyllosilicates on Mars and implications for early Martian climate. Nature 438, 623627.CrossRefGoogle ScholarPubMed
Preston, LJ, Johnson, D, Cockell, CS and Grady, MM (2015) Fourier transform infrared spectral detection of life in polar subsurface environments and its application to Mars exploration. Applied Spectroscopy 69, 10591065.CrossRefGoogle ScholarPubMed
Rabbow, E, Rettberg, P, Parpart, A, Panitz, C, Schulte, W, Molter, F and Willnecker, R (2017) EXPOSE-R2: the astrobiological ESA mission on board of the international space station. Frontiers in Microbiology 8, 114.CrossRefGoogle ScholarPubMed
Rosas, ÁL, Nosanchuk, JD, Gómez, BL, Edens, WA, Henson, JM and Casadevall, A (2000) Isolation and serological analyses of fungal melanins. Journal of Immunological Methods 244, 6980.CrossRefGoogle ScholarPubMed
Rull, F, Maurice, S, Hutchinson, I, Moral, A, Perez, C, Diaz, C and Forni, O (2017) The Raman laser spectrometer for the ExoMars rover mission to Mars. Astrobiology 17, 627654.CrossRefGoogle Scholar
Rummel, JD, Beaty, DW, Jones, MA, Bakermans, C, Barlow, NG, Boston, PJ, Chevrier, VF, Clark, BC, de Vera, J-PP, Gough, RV, Hallsworth, JE, Head, JW, Hipkin, VJ, Kieft, TL, McEwen, AS, Mellon, MT, Mikucki, JA, Nicholson, WL, Omelon, CR and Wray, JJ (2014) A new analysis of Mars "Special Regions": Findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14(11), 887–968.CrossRefGoogle Scholar
Selbmann, L, De Hoog, GS, Mazzaglia, A, Friedmann, EI and Onofri, S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Studies in Mycology 51, 132.Google Scholar
Shurvell, HF (2006) Spectra-structure correlations in the mid- and far-infrared. In Chalmers, JM and Griffiths PR (ed). Handbook of Vibrational Spectroscopy. John Wiley & Sons, Ltd. https://doi.org/10.1002/0470027320.s4101.Google Scholar
Stamenković, V, Ward, LM, Mischna, M and Fischer, WW (2018) O2 solubility in Martian near-surface environments and implications for aerobic life. Nature Geoscience 11, 905909.CrossRefGoogle Scholar
Summons, RE, Albrecht, P, McDonald, G and Moldowan, JM (2008) Molecular Biosignatures. Boston, MA: Springer, pp. 133159.Google Scholar
Thiel, CS, Pletser, V and Foing, B (2011) Human crew-related aspects for astrobiology research. International Journal of Astrobiology 10, 255267.CrossRefGoogle Scholar
Trevors, JT (2003) Possible origin of a membrane in the subsurface of the Earth. Cell Biology International 27, 451457.CrossRefGoogle Scholar
Vago, J, Witasse, O, Svedhem, H, Baglioni, P, Haldemann, A, Gianfiglio, G and de Groot, R (2015) ESA ExoMars program: the next step in exploring Mars. Solar System Research 49, 518528.CrossRefGoogle Scholar
Vago, JL, Westall, F, Coates, AJ, Jaumann, R, Korablev, O, Ciarletti, V and Rull, F (2017) Habitability on early Mars and the search for biosignatures with the ExoMars rover. Astrobiology 17, 471510.CrossRefGoogle ScholarPubMed
Vago, JL, Coates, AJ, Jaumann, R, Korablev, O, Ciarletti, V, Mitrofanov, I and Rull, F (2018) Searching for traces of life with the ExoMars rover. In From Habitability to Life on Mars. NE: Elsevier, pp. 309347.CrossRefGoogle Scholar
Vestal, JR and White, DC (1989) Lipid analysis in microbial ecology. Bioscience 39, 535541.CrossRefGoogle ScholarPubMed
Vilgalys, R and Hester, M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172, 42384246.CrossRefGoogle ScholarPubMed
Volkman, JK and Brown, MR (2006) Nutritional value of microalgae and applications. Algal cultures, analogues of blooms and applications, Inc New Hampsh. 407457.Google Scholar
Williams, AJ, Eigenbrode, J, Floyd, M, Wilhelm, MB, O'Reilly, S, Johnson, SS, Craft, KL, Knudson, CA, Andrejkovičová, S, Lewis, JMT, Buch, A, Glavin, DP, Freissinet, C, Williams, RH, Szopa, C, Millan, M, Summons, RE, McAdam, A, Benison, K, Navarro-González, R, Malespin, C and Mahaffy, PR (2019) Recovery of fatty acids from mineralogic Mars analogs by TMAH thermochemolysis for the sample analysis at Mars wet chemistry experiment on the Curiosity Rover. Astrobiology 522546. http://doi.org/10.1089/ast.2018.1819.CrossRefGoogle ScholarPubMed
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