Skip to main content

Degradation of microbial fluorescence biosignatures by solar ultraviolet radiation on Mars

  • Lewis R. Dartnell (a1) (a2) (a3) and Manish R. Patel (a4)

Recent and proposed robotic missions to Mars are equipped with implements to expose or excavate fresh material from beneath the immediate surface. Once brought into the open, any organic molecules or potential biosignatures of present or past life will be exposed to the unfiltered solar ultraviolet (UV) radiation and face photolytic degradation over short time courses. The key question, then, is what is the window of opportunity for detection of recently exposed samples during robotic operations? Detection of autofluorescence has been proposed as a simple method for surveying or triaging samples for organic molecules. Using a Mars simulation chamber we conduct UV exposures on thin frozen layers of two model microorganisms, the radiation-resistant polyextremophile Deinococcus radiodurans and the cyanobacterium Synechocystis sp. PCC 6803. Excitation–emission matrices (EEMs) are generated of the full fluorescence response to quantify the change in signal of different cellular fluorophores over Martian equivalent time. Fluorescence of Deinococcus cells, protected by a high concentration of carotenoid pigments, was found to be relatively stable over 32 h of Martian UV irradiation, with around 90% of the initial signal remaining. By comparison, fluorescence from protein-bound tryptophan in Synechocystis is much more sensitive to UV photodegradation, declining to 50% after 64 h exposure. The signal most readily degraded by UV irradiation is fluorescence of the photosynthetic pigments – diminished to only 35% after 64 h. This sensitivity may be expected as the biological function of chlorophyll and phycocyanin is to optimize the harvesting of light energy and so they are readily photobleached. A significant increase in a ∼450 nm emission feature is interpreted as accumulation of fluorescent cellular degradation products from photolysis. Accounting for diurnal variation in Martian sunlight, this study calculates that frozen cellular biosignatures would remain detectable by fluorescence for at least several sols; offering a sufficient window for robotic exploration operations.

Corresponding author
Hide All
Alberts, J. & Takács, M. (2004). Comparison of the natural fluorescence distribution among size fractions of terrestrial fulvic and humic acids and aquatic natural organic matter. Organ. Geochem. 35(10), 11411149.
Ammor, M. (2007). Recent advances in the use of intrinsic fluorescence for bacterial identification and characterization. J. Fluoresc. 17(5), 455459.
Banala, S., Moser, S., Müller, T., Kreutz, C., Holzinger, A., Lütz, C. & Kräutler, B. (2010). Hypermodified fluorescent chlorophyll catabolites: source of blue luminescence in senescent leaves. Angew. Chemi. Inter. Ed. 49(30), 5014.
Banerjee, M., Sinha, R.P. & Hader, D.-P. (1998). Biochemical and Spectroscopic Changes in Phycobiliproteins of the Cyanobacterium, Aulosira fertilissima, induced by UV-B Radiation. Acta Protozool. 37(3), 145148.
Baumstark-Khan, C. & Facius, R. (2001). Life under Conditions of Ionizing Radiation. Astrobiol., Quest Cond. Life 260283.
Carbonneau, M., Melin, A., Perromat, A. & Clerc, M. (1989). The action of free radicals on Deinococcus radiodurans carotenoids. Arch. Biochem. Biophys. 275(1), 244251.
Castenholz, R. (1988). Culturing methods for cyanobacteria. Methods Enzymol. 167, 6893.
Coble, P. (1996). Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar. Chem. 51(4), 325346.
Cockell, C. & Knowland, J. (1999). Ultraviolet radiation screening compounds. Biol. Rev. 74(3), 311345.
Cockell, C. & Raven, J. (2004). Zones of photosynthetic potential on Mars and the early Earth. Icarus 169(2), 300.
Cockell, C., Schuerger, A., Billi, D., Friedmann, E. & Panitz, C. (2005). Effects of a simulated Martian UV flux on the Cyanobacterium, Chroococcidiopsis sp. 029. Astrobiology 5(2), 127140.
Cockell, C., Catling, D.C., Davis, W.L., Snook, K., Kepner, R., Lee, P. & Mckay, C.P. (2000). The Ultraviolet Environment of Mars: Biological Implications Past, Present, and Future. Icarus 146, 343359.
Cordoba-Jabonero, C., Zorzano, M., Selsis, F., Patel, M. & Cockell, C. (2005). Radiative habitable zones in Martian polar environments. Icarus 175(2), 360371.
Cory, & McKnight, (2005). Fluorescence Spectroscopy Reveals Ubiquitous Presence of Oxidized and Reduced Quinones in Dissolved Organic Matter. Environmental Science & Technology 39(21), 81428149.
Dartnell, L.R. (2011). Ionizing radiation and life. Astrobiology 11(6), 551582.
Dartnell, L.R., Desorgher, L., Ward, J. & Coates, A. (2007a). Modelling the surface and subsurface Martian radiation environment: implications for Astrobiology. Geophys. Res. Lett. 34(2), L02207.
Dartnell, L.R., Desorgher, L., Ward, J.M. & Coates, A.J. (2007b). Martian sub-surface ionising radiation: biosignatures and geology. Biogeosciences 4, 545558.
Dartnell, L.R., Storrie-Lombardi, M.C. & Ward, J.M. (2010). Complete fluorescent fingerprints of extremophilic and photosynthetic microbes. Int. J. Astrobiol. 9(4), 245257.
Dartnell, L.R., Storrie-Lombardi, M., Mullineaux, C., Ruban, A., Wright, G., Griffiths, A., Muller, J.-P. & Ward, J. (2011). Degradation of cyanobacterial biosignatures by ionizing radiation. Astrobiology 11(10), 9971016.
Dartnell, L.R., Patel, M., Storrie-Lombardi, M.C., Ward, J.M. & Muller, J.-P. (2012). Experimental determination of photostability and fluorescence-based detection of PAHs on the Martian surface. Meteorit. Planet. Sci. 47(5), 806819.
Edgett, K., Ravine, M. & Caplinger, M. (2009). The Mars Science Laboratory (MSL) Mars Hand Lens Imager (MAHLI) Flight Instrument. In 40th Lunar and Planetary Science Conf. (Lunar and Planetary Science XL), The Woodlands, Texas, held 23–27 March, 2009, id.1197.
Ellery, A. & Wynn-Williams, D. (2003). Why Raman Spectroscopy on Mars? A case of the right tool for the right job. Astrobiology 3(3), 565579.
Evans-Nguyen, T., Becker, L., Doroshenko, V. & Cotter, R. (2008). Development of a low power, high mass range mass spectrometer for Mars surface analysis. Int. J. Mass Spectrom. 278(2–3), 170177.
Friedmann, E. (1986). The antarctic cold desert and the search for traces of life on Mars. Adv. Space Res. 6(12), 265268.
Goesmann, F., Becker, L. & Raulin, F. (2009). MOMA, the search for organics of the ExoMars mission. EPSC Abstr. 4, EPSC2009-624.
Gorevan, S. et al. (2003). Rock abrasion tool: Mars exploration rover mission. J. Geophys. Res. 108(E12), 8068.
Griffiths, A., Coates, A., Muller, J.-P., Storrie-Lombardi, M., Jaumann, R., Josset, J.-L., Paar, G. & Barnes, D. (2008). Enhancing the effectiveness of the ExoMars PanCam instrument for astrobiology. Geophys. Res. Abstr. 10, EGU2008-A-09486.
Hua, B., Dolan, F., Mcghee, C., Clevenger, T.E. & Deng, B. (2007). Water-source characterization and classification with fluorescence EEM spectroscopy: PARAFAC analysis. Int. J. Environ. Anal. Chem. 87(2), 135147.
JiJi, R., Cooper, G. & Booksh, K. (1999). Excitation-emission matrix fluorescence based determination of carbamate pesticides and polycyclic aromatic hydrocarbons. Anal. Chim. Acta 397(1–3), 6172.
Jorge Villar, S. & Edwards, H. (2006). Raman spectroscopy in astrobiology. Anal. Bioanal. Chem. 384(1), 100113.
Keränen, M., Aro, E.-M. & Tyystjärvi, E. (1999). Excitation-Emission Map as a Tool in Studies of Photosynthetic Pigment-Protein Complexes. Photosynthetica 37(2), 225237.
Ko, E., Lee, C., Kim, Y. & Kim, K. (2003). Monitoring PAH-contaminated soil using laser-induced fluorescence (LIF). Environ. Technol. 24(9), 11571164.
Kräutler, B., Banala, S., Moser, S., Vergeiner, C., Müller, T., Lütz, C. & Holzinger, A. (2010). A novel blue fluorescent chlorophyll catabolite accumulates in senescent leaves of the peace lily and indicates a split path of chlorophyll breakdown. FEBS Lett. 584(19), 42154221.
Lemee, L., Peuchant, E., Clerc, M., Brunner, M. & Pfander, H. (1997). Deinoxanthin: a new carotenoid isolated from Deinococcus radiodurans. Tetrahedron 53(3), 919926.
Mahaffy, P. et al. (2012). The sample analysis at Mars investigation and instrument suite. Space Sci. Rev. 170(1–4), 401478.
Marshall, C. & Olcott Marshall, A. (2010). The potential of Raman spectroscopy for the analysis of diagenetically transformed carotenoids. Phil. Trans. R. Soc. A, Math. Phys. Eng. Sci. 368(1922), 31373144.
Moser, S., Müller, T., Ebert, M.-O., Jockusch, S., Turro, N.J. & Kräutler, B. (2008). Blue luminescence of ripening bananas. Angew. Chem. Int. Ed. 47(46), 89548957.
Moser, S., Müller, T., Holzinger, A., Lütz, C., Jockusch, S., Turro, N. & Kräutler, B. (2009). Fluorescent chlorophyll catabolites in bananas light up blue halos of cell death. Proc. Natl. Acad. Sci. USA 106(37), 1553815543.
Muller, J.-P., Storrie-Lombardi, M. & Fisk, M. (2009). WALI – Wide Angle Laser Imaging enhancement to ExoMars PanCam: a system for organics and life detection. EPSC Abstr. 4, EPSC2009-2674-2001.
Nadeau, J., Perreault, N., Niederberger, T., Whyte, L., Sun, H. & Leon, R. (2008). Fluorescence microscopy as a tool for in situ life detection. Astrobiology 8(4), 859874.
Okon, A.B. (2010). Mars Science Laboratory Drill. In Proc. 40th Aerospace Mechanisms Symp., NASA Kennedy Space Center, 12–14 May, 2010, p 116.
Olsson-Francis, K. & Cockell, C. (2010). Experimental methods for studying microbial survival in extraterrestrial environments. J. Microbiol. Methods 80(1), 113.
Patel, M., Zarnecki, J. & Catling, D. (2002). Ultraviolet radiation on the surface of Mars and the Beagle 2 UV sensor. Planet. Space Sci. 50(9), 915927.
Patel, M., Bérces, A., Kerékgyárto, T., Rontó, G., Lammer, H. & Zarnecki, J. (2004). Annual solar UV exposure and biological effective dose rates on the Martian surface. Adv. Space Res. 33(8), 12471252.
Patra, D. & Mishra, A. (2001). Investigation on simultaneous analysis of multicomponent polycyclic aromatic hydrocarbon mixtures in water samples: a simple synchronous fluorimetric method. Talanta 55(1), 143153.
Pavlov, A., Blinov, A. & Konstantinov, A. (2002). Sterilization of Martian surface by cosmic radiation. Planet. Space Sci. 50(7–8), 669673.
Rohde, R. & Price, P. (2007). Diffusion-controlled metabolism for long-term survival of single isolated microorganisms trapped within ice crystals. Proc. Natl. Acad. Sci.USA 104(42), 1659216597.
Rull, F. et al. (2010). ExoMars Raman laser spectrometer overview. Proc. SPIE 7819(1), 781911–15.
Sims, M., Cullen, D., Bannister, N., Grant, W., Henry, O., Jones, R., McKnight, D., Thompson, D. & Wilson, P. (2005). The specific molecular identification of life experiment (SMILE). Planet. Space Sci. 53(8), 781791.
Sinha, R., Richter, P., Faddoul, J., Braun, M. & Hader, D.-P. (2002). Effects of UV and visible light on cyanobacteria at the cellular level. Photochem. Photobiol. Sci. 1(8), 553559.
Sinha, R.P., Kumar, H.D., Kumar, A. & Hader, D.-P. (1995). Effects of UV-B irradiation on growth, survival, pigmentation and nitrogen metabolism enzymes in cyanobacteria. Acta Protozool. 34(3), 187192.
Sohn, M., Himmelsbach, D., Barton, F. & Fedorka-Cray, P. (2009). Fluorescence spectroscopy for rapid detection and classification of bacterial pathogens. Appl. Spectrosc. 63(11), 12511255.
Storrie-Lombardi, M., Muller, J., Fisk, M., Griffiths, A. & Coates, A. (2008). Potential for non-destructive astrochemistry using the ExoMars PanCam. Geophys. Res. Lett. 35, L12201.
Storrie-Lombardi, M. & Sattler, B. (2009). Laser-Induced Fluorescence Emission (L.I.F.E.): in situ nondestructive detection of microbial life in the ice covers of Antarctic Lakes. Astrobiology 9(7), 659672.
Storrie-Lombardi, M., Muller, J.-P., Fisk, M., Cousins, C., Sattler, B., Griffiths, A. & Coates, A. (2009). Laser-Induced Fluorescence Emission (L.I.F.E.): searching for Mars organics with a UV-enhanced PanCam. Astrobiology 9(10), 953964.
Vago, J., Gardini, B., Kminek, G., Baglioni, P., Gianfiglio, G., Santovincenzo, A., Bayon, S. & van Winnendael, M. (2006). ExoMars: searching for Life on the Red Planet. ESA Bull. 126, 1723.
Warren, S.G. (1984). Optical constants of ice from the ultraviolet to the microwave. Appl. Opt. 23(8), 12061225.
Weinstein, S. et al. (2008). Application of pulsed-excitation fluorescence imager for daylight detection of sparse life in tests in the Atacama Desert. J. Geophys. Res. 113(G1), G01S90.
Wynn-Williams, D.D. & Edwards, H.G.M. (2000). Antarctic ecosystems as models for extraterrestrial surface habitats. Planet. Space Sci. 48, 10651075.
Ziegmann, M., Abert, M., Müller, M. & Frimmel, F.H. (2010). Use of fluorescence fingerprints for the estimation of bloom formation and toxin production of Microcystis aeruginosa. Water Res. 48, 195204.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

International Journal of Astrobiology
  • ISSN: 1473-5504
  • EISSN: 1475-3006
  • URL: /core/journals/international-journal-of-astrobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 3
Total number of PDF views: 76 *
Loading metrics...

Abstract views

Total abstract views: 239 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 17th July 2018. This data will be updated every 24 hours.