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Complete fluorescent fingerprints of extremophilic and photosynthetic microbes

Published online by Cambridge University Press:  21 July 2010

Lewis R. Dartnell*
Affiliation:
UCL Institute for Origins, University College London, UK The Centre for Planetary Sciences at UCL/Birkbeck, University College London, UK
Michael C. Storrie-Lombardi
Affiliation:
Kinohi Institute, Pasadena, California, USA
John M. Ward
Affiliation:
Structural and Molecular Biology, University College London, UK

Abstract

The work reported here represents a study into the total fluorescence exhibited by a broad selection of model, extremophilic and photosynthetic bacterial strains, over a great range of excitation and emission wavelengths from ultraviolet (UV) through visible to near infrared. The aim is to identify distinctive fluorescent features that may serve as detectable biosignatures of remnant microbial life on the Martian surface. A lab-bench fluorescence spectrometer was used to generate an excitation–emission matrix (EEM) for the unpigmented Escherichia coli, radiation-resistant Deinococcus radiodurans, Antarctic Dry Valley isolates Brevundimonas sp. MV.7 and Rhodococcus sp. MV.10, and the cyanobacterium Synechocystis sp. PCC 6803. Detailed EEMs, representing the fluorescence signature of each organism, are presented, and the most significant features suitable for biosignature surveys are identified, including small-molecule cellular metabolites, light-harvesting photosynthetic pigments and extracellular UV-screening compounds. E. coli exhibits the most intense emission from tryptophan, presumably due to the absence of UV-screening pigments that would shield the organism from short-wavelength light-exciting intracellular fluorescence. The efficacy of commonly available laser diodes for exciting cellular fluorescence is treated, along with the most appropriate filter wavelengths for imaging systems. The best combination of available laser diodes and PanCam filters aboard the ExoMars probe is proposed. The possibility of detecting fluorescence excited by solar UV radiation in freshly exposed surface samples by imaging when both sunlit and shadowed, perhaps by the body of the rover itself, is discussed. We also study how these biological fluorophore molecules may be degraded, and thus the potential biosignatures erased, by the high flux of far-ultraviolet light on Mars.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

Ajlani, G., Vernotte, C., DiMagno, L. & Haselkorn, R. (1995). Biochim. Biophys. Acta Bioenerg. 1231(2), 189196.CrossRefGoogle Scholar
Alberts, J. & Takács, M. (2004). Org. Geochem. 35(10), 11411149.CrossRefGoogle Scholar
Anderson, A., Nordan, H., Cain, R., Parrish, G. & Duggan, D. (1956). Food Tech. 10(1), 575577.Google Scholar
Asher, S. (1993). Anal. Chem. 65(2), 59A66A.CrossRefGoogle Scholar
Battistuzzi, F. & Hedges, S. (2009). Mol. Biol. Evol. 26(2), 335343.CrossRefGoogle Scholar
Bell, J. et al. (2003). J. Geophys. Res. 108(E12), 8063.Google Scholar
Bhartia, R. et al. (2008). Appl. Spectros. 62(10), 10701077.CrossRefGoogle Scholar
Billi, D., Friedmann, E., Hofer, K., Caiola, M. & Ocampo-Friedmann, R. (2000). Appl. Environ. Microbiol. 66(4), 14891492.CrossRefGoogle Scholar
Blinks, L. (1954). Annu. Rev. Plant Physiol. 5(1), 93–114.CrossRefGoogle Scholar
Brettell, T. & Saferstein, R. (1991). Anal. Chem. 63(12), 148R164R.CrossRefGoogle Scholar
Campbell, L. & Iturriaga, R. (1988). Limnol. Oceanogr. 33(5), 11961201.CrossRefGoogle Scholar
Castenholz, R. (1988). Meth Enzymol. 167, 6893.CrossRefGoogle Scholar
Chatterley, C. & Linden, K. (2010). J. Water Health 8(3), 479.CrossRefGoogle Scholar
Cockell, C. (2000). Icarus 146, 343359.CrossRefGoogle Scholar
Cox, M. & Battista, J. (2005). Nat. Rev. Microbiol. 3(11), 882892.CrossRefGoogle Scholar
Daly, M. et al. (2004). Science 306(5698), 10251028.CrossRefGoogle Scholar
Dartnell, L., Desorgher, L., Ward, J. & Coates, A. (2007a). Biogeosciences 4, 545558.CrossRefGoogle Scholar
Dartnell, L., Desorgher, L., Ward, J. & Coates, A. (2007b). Geophys. Res. Lett. 34(2), L02207.CrossRefGoogle Scholar
Dartnell, L., Hunter, S., Lovell, K., Coates, A. & Ward, J. (2010). Astrobiology in press.Google Scholar
Diagaradjane, P., Yaseen, M., Yu, J., Wong, M. & Anvari, B. (2005). Laser. Surg. Med. 37(5), 382395.CrossRefGoogle Scholar
Edwards, H. (2007). Origins Life Evol. Biosphere 37(4), 335339.CrossRefGoogle Scholar
Elliott, S., Lead, J. & Baker, A. (2006). Water Res. 40(10), 20752083.CrossRefGoogle Scholar
Erokhina, L., Shatilovich, A., Kaminskaya, O. & Gilichinskii, D. (2002). Microbiology 71(5), 601607.CrossRefGoogle Scholar
Fisk, M., Storrie-Lombardi, M., Douglas, S., Popa, R., McDonald, G. & Di Meo-Savoie, C. (2003). Geochem. Geophys. Geosyst. 4(12), 1103.CrossRefGoogle Scholar
Friedmann, E. (1982). Science 215(4536), 10451053.CrossRefGoogle Scholar
Friedmann, E. (1986). Adv. Space Res. 6(12), 265268.CrossRefGoogle Scholar
Friedmann, E. & Ocampo, R. (1976). Science 193(4259), 12471249.CrossRefGoogle Scholar
Garcia-Pichel, F. (1998). Origins Life Evol. Biosphere 28(3), 321347.CrossRefGoogle Scholar
Garcia-Pichel, F. & Castenholz, R. (1991). J. Phycol. 27(3), 395409.CrossRefGoogle Scholar
Garcia-Pichel, F., Sherry, N. & Castenholz, R. (1992). Photochem. Photobiol. 56(1), 1723.CrossRefGoogle Scholar
Georgakoudi, I. et al. (2002). Cancer Res. 62(3), 682687.Google Scholar
Gilichinsky, D. (2007). Astrobiology 7(2), 275311.CrossRefGoogle ScholarPubMed
Gilichinsky, D., Vorobyova, E., Erokhina, L., Fyordorov-Dayvdov, D. & Chaikovskaya, N. (1992). Adv. Space Res. 12(4), 255263.CrossRefGoogle Scholar
Glazer, A. (1985). Annu. Rev. Biophys. Biophys. Chem. 14(1), 4777.CrossRefGoogle Scholar
Griffiths, A., Coates, A., Josset, J., Paar, G., Hofmann, B., Pullan, D., Rüffer, P., Sims, M., Pillinger, C. (2005). Planet Space Sci. 53(14–15), 14661482.CrossRefGoogle Scholar
Griffiths, A., Coates, A., Jaumann, R., Michaelis, H., Paar, G., Barnes, D., Josset, J-L., and the PanCam, Team (2006). Int. J. Astrobiol. 5(3), 269275.CrossRefGoogle Scholar
Griffiths, A., Coates, A., Muller, J-P., Storrie-Lombardi, M., Jaumann, R., Josset, J-L., Paar, G., Barnes, D. (2008). Geophys. Res. Abstr. 10:EGU2008-A-09486.Google Scholar
Hirayama, H., Yatabe, T., Noguchi, N. & Kamata, N. (2010). Electron. Commun. Jpn. 93(3), 2433.CrossRefGoogle Scholar
Hoge, F. & Swift, R. (1981). Appl. Opt. 20(18), 31973205.CrossRefGoogle Scholar
Horneck, G. (2000). Planet. Space Sci. 48(11), 1053.CrossRefGoogle Scholar
Kim, H.Y., Estes, C.R., Duncan, A.G., Wade, B.D., Cleary, F.C., Lloyd, C.R., Ellis, W.R. Jr, Powers, L.S. (2004). IEEE Eng. Med. Biol. Mag. 23(1), 122129.Google Scholar
Klapper, L., McKnight, D., Fulton, J., Blunt-Harris, E., Nevin, K., Lovley, D., Hatcher, P. (2002). Environ. Sci. Technol. 36(14), 31703175.CrossRefGoogle Scholar
Latifi, A., Ruiz, M. & Zhang, C.-C. (2009). FEMS Microbiol. Rev. 33, 258278.CrossRefGoogle Scholar
MacColl, R. (1998). J. Struct. Biol. 124(2–3), 311334.CrossRefGoogle Scholar
Malin, M. et al. (2005). The Mast Cameras and Mars Descent Imager (MARDI) for the 2009 Mars Science Laboratory. In Proc. 36th Annual Lunar and Planetary Science Conf., vol. 36, p. 1214.Google Scholar
Muller, J.-P., Storrie-Lombardi, M. & Fisk, M. (2009). EPSC Abstr. 4, EPSC2009-674-1.Google Scholar
Nealson, K., Tsapin, A. & Storrie-Lombardi, M. (2002). Int. Microbiol. 5(4), 223230.Google Scholar
Oldbam, P., Zillioux, E. & Warner, I. (1985). J. Mar. Res. 43, 893906.CrossRefGoogle Scholar
Packer, L. & Glazer, A. (1988). Meth. Enzymol. 167, 304312.Google Scholar
Palmer, G., Keely, P., Breslin, T. & Ramanujam, N. (2003). Photochem. Photobiol. 78(5), 462469.2.0.CO;2>CrossRefGoogle Scholar
Patel, M., Zarnecki, J. & Catling, D. (2002). Planet. Space Sci. 50(9), 915927.CrossRefGoogle Scholar
Pointing, S., Chan, Y., Lacap, D., Lau, M., Jurgens, J., Farrell, R. (2009). Proc. Nat. Acad. Sci. USA 106(47), 1996419969.CrossRefGoogle Scholar
Price, P. (2007). FEMS Microbiol. Ecol. 59(2), 217231.CrossRefGoogle Scholar
Priscu, J. et al. (1998). Science 280(5372), 20952098.CrossRefGoogle Scholar
Proteau, P., Gerwick, W., Garcia-Pichel, F. & Castenholz, R. (1993). Cell. Mol. Life Sci. 49(9), 825829.CrossRefGoogle Scholar
Richmond, R., Sridhar, R. & Daly, M. (1999). Physicochemical survival pattern for the radiophile Deinococcus radiodurans: A polyextremophile model for life on Mars. In Proc. SPIE Conf. on Instruments, Methods, and Missions for Astrobiology II, vol. 3755, pp. 210222.Google Scholar
Rohde, R., Price, P., Bramall, N. & Bay, R. (2007). Eos Trans. AGU 88(52).Google Scholar
Ronto, G., Berces, A., Lammer, H., Cockell, C., Molina-Cuberos, G., Patel, M., Selsis, F. (2003). Photochem. Photobiol. 77(1), 3440.CrossRefGoogle Scholar
Samsonoff, W. & MacColl, R. (2001). Arch. Microbiol. 176(6), 400405.CrossRefGoogle Scholar
Senesi, N., Miano, T., Provenzano, M. & Brunetti, G. (1989). Sci. Total Environ. 81–82, 143156.CrossRefGoogle Scholar
Smith, P. et al. (1997). J. Geophys. Res. 102(E2), 40034025.CrossRefGoogle Scholar
Sohn, M., Himmelsbach, D., Barton, F. & Fedorka-Cray, P. (2009). Appl. Spectros. 63(11), 12511255.CrossRefGoogle Scholar
Storrie-Lombardi, M. (2005). Post-Bayesian strategies to optimize astrobiology instrument suites: lessons from Antarctica and the Pilbara. In Astrobiology and Planetary Missions, ed. Hoover, R.B., Levin, G.V. & Rozanov, A.Y.SPIE, Bellingham, WA.Google Scholar
Storrie-Lombardi, M., Hug, W., McDonald, G., Tsapin, A. & Nealson, K. (2001). Rev. Sci. Instrum. 72(12), 44524459.CrossRefGoogle Scholar
Storrie-Lombardi, M., Muller, J., Fisk, M., Griffiths, A. & Coates, A. (2008). Geophys. Res. Lett. 35.CrossRefGoogle Scholar
Storrie-Lombardi, M., Muller, J.P., Fisk, M., Cousins, C., Sattler, B., Griffiths, A., Coates, A. (2009). Astrobiology 9(10), 953964.CrossRefGoogle Scholar
Thornley, M., Horne, R. & Glauert, A. (1965). Arch. Mikrobiol. 51(3), 267289.CrossRefGoogle Scholar
Twardowski, M., Mouw, C., Dombroski, J. & Smith, D. (2007). Discriminating organic chemical signatures in interstitial waters of deeply buried sediments using fluorescence spectroscopy. In American Geophysical Union Fall Meeting Abstracts.Google Scholar
Vago, J., Gardini, B., Kminek, G., Baglioni, P., Gianfiglio, G., Santovincenzo, A., Bayon, S., van Winnendael, M. (2006). ESA Bull. 126, 1723.Google Scholar
Wynn-Williams, D. & Edwards, H. (2000). Icarus 144(2), 486503.CrossRefGoogle Scholar
Zhang, Q.-Q., Lei, S.-H., Wang, X.-L., Wang, L. & Zhu, C.-J. (2006). Spectrochim. Acta Part A 63, 361369.CrossRefGoogle Scholar
Ziegmann, M., Abert, M., Müller, M. & Frimmel, F. (2010). Water Res. 44, 195204.CrossRefGoogle Scholar