Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T03:58:07.911Z Has data issue: false hasContentIssue false

Nucleic acids and melanin pigments after exposure to high doses of gamma rays: a biosignature robustness test

Published online by Cambridge University Press:  06 July 2022

A. Cassaro
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
C. Pacelli*
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy Human Spaceflight and Scientific Research Unit, Italian Space Agency, via del Politecnico snc, Rome, Italy
M. Baqué
Affiliation:
Planetary Laboratories Department, German Aerospace Center (DLR e.V.), Institute of Planetary Research, Rutherfordstraße 2, Berlin, Germany
A. Maturilli
Affiliation:
Planetary Laboratories Department, German Aerospace Center (DLR e.V.), Institute of Planetary Research, Rutherfordstraße 2, Berlin, Germany
U. Boettger
Affiliation:
German Aerospace Center (DLR e.V.), Institute of Optical Sensor Systems, Rutherfordstraße 2, Berlin, Germany
R. Moeller
Affiliation:
Radiation Biology Department, Aerospace Microbiology, German Aerospace Center (DLR e.V.), Institute of Aerospace Medicine, Cologne (Köln), Germany Department of Natural Sciences, University of Applied Sciences Bonn-Rhein-Sieg (BRSU), Rheinbach, Germany
A. Fujimori
Affiliation:
Molecular and Cellular Radiation Biology Group, Department of Basic Medical Sciences for Radiation Damages, NIRS/QST, Chiba, Japan
J-P.P. de Vera
Affiliation:
German Aerospace Center (DLR e.V.), MUSC, Space Operations and Astronaut Training, Linder Höhe, Cologne, Germany
S. Onofri
Affiliation:
Department of Ecological and Biological Sciences, University of Tuscia, Largo dell'Università snc, 01100 Viterbo, Italy
*
Author for correspondence: C. Pacelli, E-mail: [email protected]

Abstract

The question about the stability of certain biomolecules is directly connected to the life-detection missions aiming to search for past or present life beyond Earth. The extreme conditions experienced on extraterrestrial planet surface (e.g. Mars), characterized by ionizing and non-ionizing radiation, CO2-atmosphere and reactive species, may destroy the hypothetical traces of life. In this context, the study of the biomolecules behaviour after ionizing radiation exposure could provide support for the onboard instrumentation and data interpretation of the life exploration missions on other planets. Here, as a part of STARLIFE campaign, we investigated the effects of gamma rays on two classes of fungal biomolecules–nucleic acids and melanin pigments – considered as promising biosignatures to search for during the ‘in situ life-detection’ missions beyond Earth.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aureli, L, Pacelli, C, Cassaro, A, Fujimori, A, Moeller, R and Onofri, S (2020) Iron ion particle radiation resistance of dried colonies of Cryomyces antarcticus embedded in Martian regolith analogues. Life 10, 306.CrossRefGoogle ScholarPubMed
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
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. Radiation Research 180, 622637.CrossRefGoogle ScholarPubMed
Biemann, K, Oro, JIIIPT, Toulmin, P III, Orgel, LE, Nier, AO, Anderson, DM and Lafleur, AL (1977) The search for organic substances and inorganic volatile compounds in the surface of Mars. Journal of Geophysical Research 82, 46414658.CrossRefGoogle Scholar
Bonneville, S, Delpomdor, F, Préat, A, Chevalier, C, Araki, T, Kazemian, M and Benning, LG (2020) Molecular identification of fungi microfossils in a Neoproterozoic shale rock. Science Advances 6, eaax7599.CrossRefGoogle Scholar
Briggs, AW, Good, JM, Green, RE, Krause, J, Maricic, T, Stenzel, U and Pääbo, S (2009) Primer extension capture: targeted sequence retrieval from heavily degraded DNA sources. JoVE (Journal of Visualized Experiments) 31, e1573.Google Scholar
Carbone, I and Kohn, LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91, 553556.CrossRefGoogle Scholar
Cassaro, A, Pacelli, C, Aureli, L, Catanzaro, I, Leo, P and Onofri, S (2021 a) Antarctica As a reservoir of planetary analogue environments. Extremophiles 25, 437458.CrossRefGoogle ScholarPubMed
Cassaro, A, Pacelli, C, Baqué, M, de Vera, JPP, Böttger, U, Botta, L and Onofri, S (2021 b) Fungal biomarkers stability in Mars regolith analogues after simulated space and Mars-like conditions. Journal of Fungi 7, 859.CrossRefGoogle ScholarPubMed
Cassaro, A, Pacelli, C, Baqué, M, Cavalazzi, B, Gasparotto, G, Saladino, R, Botta, L, Böttger, U, Rabbow, E, de Vera, JPP and Onofri, S (2022) Investigation of fungal biomolecules after low earth orbit exposure: a testbed for the next moon missions. Environmental Microbiology.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
Dadachova, E and Casadevall, A (2008) Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Current Opinion 11, 525531.CrossRefGoogle ScholarPubMed
Dadachova, E, Bryan, RA, Huang, X, Moadel, T, Schweitzer, AD, Aisen, P and Casadevall, A (2007) Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS ONE 2, e457.CrossRefGoogle ScholarPubMed
Dartnell, LR, Desorgher, L, Ward, JM and Coates, AJ (2007) Martian sub-surface ionising radiation: biosignatures and geology. Biogeosciences 4, 545558.CrossRefGoogle Scholar
Davila, AF and McKay, CP (2014) Chance and necessity in biochemistry: implications for the search for extraterrestrial biomarkers in earth-like environments. Astrobiology 14, 534540.CrossRefGoogle ScholarPubMed
Des Marais, DJ, Nuth, JA III, Allamandola, LJ, Boss, AP, Farmer, JD, Hoehler, TM and Spormann, AM (2008) The NASA astrobiology roadmap. Astrobiology 8, 715730.CrossRefGoogle ScholarPubMed
Drake, MJ, Greeley, R, McKay, GA, Blanchard, DP, Carr, MH, Gooding, JL, McKay, CP, Spudis, PD and Squyres, SW (eds) (1988) Workshop on Mars Sample Return Science. LPI Tech. Rpt. 88-07. Houston: Lunar and Planetary Institute.Google Scholar
Ehrlich, H, Kaluzhnaya, OV, Brunner, E, Tsurkan, MV, Ereskovsky, A, Ilan, M and Wörheide, G (2013) Identification and first insights into the structure and biosynthesis of chitin from the freshwater sponge Spongilla lacustris. Journal of Structural Biology 183, 474483.CrossRefGoogle ScholarPubMed
Ferrara, MA, De Angelis, A, De Luca, AC, Coppola, G, Dale, B and Coppola, G (2016) Simultaneous holographic microscopy and Raman spectroscopy monitoring of human spermatozoa photodegradation. IEEE Journal of Selected Topics in Quantum Electronics 22, 2734.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, e0170611.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
Hassler, DM, Zeitlin, C, Wimmer-Schweingruber, RF, Ehresmann, B, Rafkin, S, Eigenbrode, JL and Berger, G (2014) Mars’ surface radiation environment measured with the Mars science laboratory's curiosity rover. Science 343, 1244797.CrossRefGoogle ScholarPubMed
Hunt, S (1970) Polysaccharide-Protein Complexes in Invertebrates. London: Academic Press.Google Scholar
Krafft, C (2004) Bioanalytical applications of Raman spectroscopy. Analytical and Bioanalytical Chemistry 378, 6062.CrossRefGoogle ScholarPubMed
Lasne, J, Noblet, A, Szopa, C, Navarro-González, R, Cabane, M, Poch, O and Coll, P (2016) Oxidants at the surface of Mars: a review in light of recent exploration results. Astrobiology 16, 977996.CrossRefGoogle Scholar
Malin, MC and Edgett, KS (2000) Sedimentary rocks of early Mars. Science 290, 19271937.CrossRefGoogle ScholarPubMed
Malo, ME and Dadachova, E (2019) Melanin as an energy transducer and a radioprotector in black fungi. In Tiquia-Arashiro, S and Grube, M (eds), Fungi in Extreme Environments: Ecological Role and Biotechnological Significance. Cham: Springer, pp. 175184.CrossRefGoogle Scholar
Mbonyiryivuze, A, Mwakikunga, BW, Dhlamini, SM and Maaza, M (2015) Fourier transform infrared spectroscopy for sepia melanin. Physics and Materials Chemistry 3, 2529.Google Scholar
McKay, CP (2004) What is life—and how do we search for it in other worlds?. PLoS Biology 2, e302.CrossRefGoogle ScholarPubMed
McKay, CP (2020) What is life—and when do we search for it on other worlds. Astrobiology 20, 163166.CrossRefGoogle ScholarPubMed
Meeßen, J, Sánchez, FJ, Sadowsky, A, de la Torre, R, Ott, S and de Vera, JP (2013) Extremotolerance and resistance of lichens: comparative studies on five species used in astrobiological research II. Secondary lichen compounds. Origins of Life and Evolution of Biospheres 43, 501526.CrossRefGoogle ScholarPubMed
Meeßen, J, Backhaus, T, Brandt, A, Raguse, M, Böttger, U, de Vera, JP and de la Torre, R (2017) The effect of high-dose ionizing radiation on the isolated photobiont of the astrobiological model lichen Circinaria gyrosa. Astrobiology 17, 154162.CrossRefGoogle ScholarPubMed
Moeller, R, Raguse, M, Leuko, S, Berger, T, Hellweg, CE and Fujimori, A and STARLIFE Research Group (2017) STARLIFE—An international campaign to study the role of galactic cosmic radiation in astrobiological model systems. Astrobiology 17, 101109.CrossRefGoogle Scholar
Movasaghi, Z, Rehman, S and Rehman, DI (2008) Fourier transform infrared (FTIR) spectroscopy of biological tissues. Applied Spectroscopy Reviews 43, 134179.CrossRefGoogle Scholar
Neveu, M, Hays, LE, Voytek, MA, New, MH and Schulte, MD (2018) The ladder of life detection. Astrobiology 18, 13751402.CrossRefGoogle ScholarPubMed
Nosanchuk, JD and Casadevall, A (2003) The contribution of melanin to microbial pathogenesis. Cellular Microbiology 5, 203223.CrossRefGoogle ScholarPubMed
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
Owen, T, Biemann, K, Rushneck, DR, Biller, JE, Howarth, DW and Lafleur, AL (1977) The composition of the atmosphere at the surface of Mars. Journal of Geophysical Research 82, 46354639.CrossRefGoogle Scholar
Pace, NR (2001) The universal nature of biochemistry. PNAS 98, 805808.CrossRefGoogle ScholarPubMed
Pacelli, C, Selbmann, L, Zucconi, L, Raguse, M, Moeller, R, Shuryak, I and Onofri, S (2017 a) Survival, DNA integrity, and ultrastructural damage in antarctic cryptoendolithic eukaryotic microorganisms exposed to ionizing radiation. Astrobiology 17, 126135.CrossRefGoogle ScholarPubMed
Pacelli, C, Bryan, RA, Onofri, S, Selbmann, L, Shuryak, I and Dadachova, E (2017 b) Melanin is effective in protecting fast and slow growing fungi from various types of ionizing radiation. Environmental Microbiology 19, 16121624.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, Selbmann, L, Zucconi, L, Coleine, C, de Vera, JP, Rabbow, E and Onofri, S (2019) Responses of the black fungus Cryomyces antarcticus to simulated Mars and space conditions on rock analogs. Astrobiology 19, 209220.CrossRefGoogle ScholarPubMed
Pacelli, C, Cassaro, A, Aureli, L, Moeller, R, Fujimori, A and Onofri, S (2020 a) The responses of the black fungus Cryomyces antarcticus to high doses of accelerated helium ions radiation within Martian regolith simulants and their relevance for Mars. Life 10, 130.CrossRefGoogle ScholarPubMed
Pacelli, C, Cassaro, A, Maturilli, A, Timperio, AM, Gevi, F, Cavalazzi, B and Onofri, S (2020 b) Multidisciplinary characterization of melanin pigments from the black fungus Cryomyces antarcticus. AMAB 104, 63856395.Google ScholarPubMed
Pacelli, C, Alessia, C, Siong, LM, Lorenzo, A, Moeller, R, Fujimori, A and Silvano, O (2021 a) Insights into the survival capabilities of Cryomyces antarcticus hydrated colonies after exposure to Fe particle radiation. Journal of Fungi 7, 495.CrossRefGoogle ScholarPubMed
Pacelli, C, Cassaro, A, Baqué, M, Selbmann, L, Zucconi, L, Maturilli, A and Onofri, S (2021 b) Fungal biomarkers are detectable in Martian rock-analogues after space exposure: implications for the search of life on Mars. International Journal of Astrobiology 20, 345358.CrossRefGoogle Scholar
Pacelli, C, Cassaro, A, Catanzaro, I, Baqué, M, Maturilli, A, Böttger, U, Botta, L, Saladino, R, Rabbow, E and Onofri, S (2021 c) The ground-based BIOMEX experiment verification tests for life detection on Mars. Life 11, 1212.CrossRefGoogle ScholarPubMed
Paim, S, Linhares, LF, Mangrich, AS and Martin, JP (1990) Characterization of fungal melanins and soil humic acids by chemical analysis and infrared spectroscopy. Biology and Fertility of Soils 10, 7276.CrossRefGoogle Scholar
Pal, AK, Gajjar, DU and Vasavada, AR (2013) DOPA And DHN pathway orchestrate melanin synthesis in Aspergillus species. Medical Mycology 52, 1018.Google Scholar
Raman, NM and Ramasamy, S (2017) Genetic validation and spectroscopic detailing of DHN-melanin extracted from an environmental fungus. Biochemistry and Biophysics Reports 12, 98107.CrossRefGoogle ScholarPubMed
Rasmussen, B, Blake, TS, Fletcher, IR and Kilburn, MR (2009) Evidence for microbial life in synsedimentary cavities from 2.75 Ga terrestrial environments. Geology 37, 423426.CrossRefGoogle Scholar
Raymond-Bouchard, I, Maggiori, C, Brennan, L, Altshuler, I, Manchado, JM, Parro, V and Whyte, LG (2022) Assessment of automated nucleic acid extraction systems in combination with MinION sequencing as potential tools for the detection of microbial biosignatures. Astrobiology 22, 87103.CrossRefGoogle ScholarPubMed
Rebrošová, K, Šiler, M, Samek, O, Růžička, F, Bernatová, S, Holá, V and Petráš, P (2017) Rapid identification of staphylococci by Raman spectroscopy. Scientific Reports 7, 18.CrossRefGoogle ScholarPubMed
Robinson, CH (2001) Cold adaptation in Arctic and Antarctic fungi. New phytolo 151, 341353.CrossRefGoogle Scholar
Salman, A, Shufan, E, Tsror, L, Moreh, R, Mordechai, S and Huleihel, M (2014) Classification of Colletotrichum coccodes isolates into vegetative compatibility groups using infrared attenuated total reflectance spectroscopy and multivariate analysis. Methods 68, 325330.CrossRefGoogle ScholarPubMed
Samokhvalov, A, Liu, Y and Simon, JD (2004) Characterization of the Fe (III)-binding site in sepia eumelanin by resonance Raman confocal microspectroscopy. Journal of Photochemistry and Photobiology 80, 8488.CrossRefGoogle ScholarPubMed
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
Selbmann, L, Pacelli, C, Zucconi, L, Dadachova, E, Moeller, R, de Vera, JP and Onofri, S (2018) Resistance of an Antarctic cryptoendolithic black fungus to radiation gives new insights of astrobiological relevance. Fungal Biology 122, 546554.CrossRefGoogle ScholarPubMed
Shurvell, HF (2006) Spectra–structure correlations in the mid-and far-infrared. In Chalmers, JM and Griffiths, PR (eds), Handbook of Vibrational Spectroscopy, vol. 1. Chichester, UK: John Wiley & Sons, Ltd, pp. 134.Google Scholar
Simpson, JA (1983) Elemental and isotopic composition of the galactic cosmic rays. Annual Review of Nuclear and Particle Science 33, 323382.CrossRefGoogle Scholar
Speranza, M, Ascaso, C, Delclòs Martínez, X and Peñalver, E (2015) Cretaceous mycelia preserving fungal polysaccharides: taphonomic and paleoecological potential of microorganisms preserved in fossil resins. Geologica Acta: An International Earth Science Journal 13, 363385.Google Scholar
Summons, RE, Albrecht, P, McDonald, G and Moldowan, JM (2008) Molecular biosignatures. In Botta, O, Bada, JL, Gomez-Elvira, J, Javaux, E, Selsis, F and Summons, R (eds). Strategies of Life Detection, Space Sciences Series of ISSI, vol. 25. Boston, MA: Springer, pp. 133159.CrossRefGoogle Scholar
Sun, S, Zhang, X, Sun, S, Zhang, L, Shan, S and Zhu, H (2016) Production of natural melanin by Auricularia auricula and study on its molecular structure. Food Chemistry 190, 801807.CrossRefGoogle Scholar
Trevors, JT (2003) Possible origin of a membrane in the subsurface of the earth. Cell Biology International 27, 451457.CrossRefGoogle ScholarPubMed
Turick, CE, Ekechukwu, AA, Milliken, CE, Casadevall, A and Dadachova, E (2011) Gamma radiation interacts with melanin to alter its oxidation–reduction potential and results in electric current production. Bioelectrochem 82, 6973.CrossRefGoogle ScholarPubMed
Vember, VV and Zhdanova, NN (2001) Peculiarities of linear growth of the melanin-containing fungi Cladosporium sphaerospermum Penz. and Alternaria alternata (Fr.) Keissler. Journal of Microbiology 63, 312.Google 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
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
Supplementary material: Image

Cassaro et al. supplementary material

Figure S1

Download Cassaro et al. supplementary material(Image)
Image 11.3 MB