Sulfur Metabolism

MTB would also take part in the sulfur cycle. In nature, sulfur is mainly found under three forms: compounds of the sulfate ion (SO42-), compounds of the sulfide ion (S2-) and elemental sulfur (S0). Sulfates are very abundant on Mars and some MTB can reduce the sulfate ion to sulfide. This biochemical process would form sulfydric acid and sulfides. Other bacterial species, such as strain MC-1, can oxidize sulfides and thiosulfates and producing elemental sulfur. The sulfide ion can be used by anoxygenic photosynthetic bacteria, including facultative anoxygenic cyanobacteria, as the electron source for cell metabolism enabling them to reduce carbon dioxide during the synthesis of organic compounds.

4. Conclusions and Future Prospects

In the new environment created by ecopoiesis, allowing autotrophic microorganisms and/or extremophilic ones to growth and multiply, MTB could play roles in carbon, oxygen, nitrogen, iron and sulfur cycles on Mars or on other planets (Fig. 1). MTB have several particularities that argue for their potential in the terraforming process, the following being the most important:

1. The ability of some MTB to fix carbon dioxide in the dark using the energy released through the oxidation of inorganic chemicals such as thiosulfate;

trophic chains trophic chains

Figure 1. The importance of magnetotactic bacteria for terraformation (for details see text).

trophic chains trophic chains

Figure 1. The importance of magnetotactic bacteria for terraformation (for details see text).

these chemolitoautotrophic MTB could be a primary source of organic carbon once molecular oxygen, even in limited concentrations, is available.

2. The ability to carry out aerobic or anaerobic respiration with either nitrate or ferric iron. The use of nitrate as the terminal electron acceptor in anaerobic respiration (nitrate respiration) by some MTB could enable them to work together with other nitrate respiring bacteria during terraformation of Mars and other planets. Nitrate respiration should be very intense during the first phases of terraforma-tion, until the atmospheric oxygen level would increase, inhibiting the process at aerobic sites and forcing nitrate-respiring bacteria to withdraw to anaerobic sites.

3. MTB together with other types of microorganisms could contribute to a nitrogen cycle on Mars, carrying out two important tasks: a constant percentage of N2 in the atmosphere (by denitrification) and the availability of this macro element to ecosystems (by nitrogen fixation).

4. MTB could consume ferric iron which, at high concentrations, is toxic for living organisms. At a neutral pH, the solubility of ferric iron is very low, but for each pH unit less, its solubility increases 1,000 times. During the first stages of terraformation of Mars, due to the CO2 atmosphere, Martian waters would be acid and ferric iron would dissolve causing problems to living cells. MTB could have a contribution in solving these problems by fixing the iron in the form of solid magnetite or greigite.

5. Magneto-aerotaxis, as well as other magnetic assisted taxies, could constitute specific advantages of MTB in their navigation toward optimum growth conditions during the process of terraformation of planets with a global magnetic field similar to that of Earth. MTB could keep this advantage even on Mars, in the regions having a local magnetism of 100 to 600 nT (http://mgs-mager.gsfc.nasa. gov; http://denali.gsfc.nasa.gov/terr_mag/index.html). In those regions containing large iron deposits in the crust, one can develop microcosms where MTB could use magneto-aerotaxis or other magnetic assisted taxies to reach the appropriate concentration of nutrients. The experiments concerning microcosms are important for terraformation as it seems rational that microcosms could be used to start up ecosystems on Mars or others planets, once ecopoiesis is established.

The improvement of our knowledge concerning the biology of MTB, including their relationship with biotic and abiotic factors, is needed for the use of MTB in the terraformation of Mars or other planets. Furthermore, genetic modification of MTB could increase their potential for terraformation by improving their relationship with autotrophic and extremophilic microorganisms as well as making them more robust to face adverse physical and chemical conditions.

5. Acknowledgments

Thanks are due to the both referees whose professional criticism and valuable suggestions helped the authors to improve the manuscript.

6. References

Averner, M. M. and MacElroy, R. D. (1976) On the habitability of Mars: an approach to planetary ecosynthesis. NASA SP-414.

Badescu, V. (2005) Regional and seasonal limitations for Mars Intrinsic Ecopoiesis. Acta Astronaut. 56, 670-680.

Barber, D. J. and Scott, E. R. D. (2002) Origin of supposedly biogenic magnetite in the Martian meteorite Allan Hills 84001. Proc. Natl. Acad. Sci. USA 99, 6556-6561.

Bazylinski, D. A. and Blakemore, R. P. (1983) Nitrogen fixation (acetylene reduction) in Aquaspirillum magnetotacticum. Curr. Microbiol. 9, 305-308.

Bazylinski, D. A. and Frankel R. B. (2004) Magnetosome formation in prokaryotes. Nat. Rev. 2, 217-230.

Bazylinski, D. A. and Moskowitz, B. M. (1997) Microbial biomineralization of magnetic iron minerals: microbiology, magnetism, and environmental significance. In: J. Banfield and K. Nealson (eds.) Geomicrobiology: Interactions Between Microbes and Minerals, vol. 35. Mineralogical Society of America, Washington, DC, pp. 181-224.

Bazylinski, D. A., Frankel, R. B., and Jannasch, H. W. (1988) Anaerobic magnetite production by a marine magnetotactic bacterium. Nature 334, 518-519.

Bazylinski, D. A., Frankel, R. B., Heywood, B. R., Mann, S., King, J. W., Donaghay, P. L., and Hanson A. K. (1995) Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Appl. Environ. Microbiol. 61, 3232-3239.

Bazylinski, D. A., Dean, A. J., Schüler, D., Phillips, E. J. P., and Lovley, D. R. (2000) N2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria Geobacter and Magnetospirillum species. Environ. Microbiol. 2, 266-273.

Bazylinski, D. A., Dean, A. J., Williams, T. J., Long, L. K., Middleton, S. L., and Dubbels, B. L. (2004) Chemolitoauto trophy in the marine, magnetotactic bacterial strains MV-1 and MV-2. Arch. Microbiol. 182, 373-387.

Bazylinski, D. A., Frankel, R. B., and Konhauser, K. O. (2007) Modes of biomineralization of magnetite by microbes. Geomicrobiol. J. 24, 465-475.

Birch, P. (1992) Terraforming Mars quickly. JBIS 45, 331-340.

Blakemore, R. P. (1975) Magnetotactic bacteria. Science 190, 377-379.

Blakemore, R. P. (1982) Magnetotactic bacteria. Annu. Rev. Microbiol. 36, 217-238.

Blakemore, R. P., Maratea, D., and Wolfe, R. S. (1979) Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J. Bacteriol. 140, 720-729.

Buseck, P. R., Dunin-Borkowski, R. E., Devouard, B., Frankel, R. B., McCartney, M. R., Midgley, P. A., Posfai, M., and Weyland, M. (2001) Magnetite morphology and life on Mars. Proc. Natl. Acad. Sci. USA 98, 13490-13495.

Butler, R. F. and Banerjee, S. K. (1975) Theoretical single-domain grain size range in magnetite and titanomagnetite. J. Geophys. Res. 80, 252-259.

Flies, C. B., Jonkers, H. M., De Beer, D., Bosselmann, K., Böttcher, M. E., and Schüler, D. (2005) Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol. Ecol. 52, 185-195.

Fogg, M. J. (1989) The Creation of an artificial, dense Martian atmosphere: a major obstacle to the terraforming of Mars. JBIS 42, 577-582.

Fogg, M. J. (1993) Terraforming: a review for environmentalists. The Environmentalist 13, 7-17.

Fogg, M. J. (1995) Terraforming: Engineering Planetary Environments. SAE International Publisher, Warrendale, PA.

Fogg, M. J. (1998) Terraforming Mars: a review of current research. Adv. Space Res. 3, 415-442.

Frankel, R. B. and Bazylinski, D. A. (2006) How magnetotactic bacteria make magnetosomes queue up. Trends Microbiol. 14, 329-331.

Frankel, R. B., Bazylinski, D. A., Johnson, M. S., and Taylor, B. L. (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys. J. 73, 994-1000.

Frankel, R. B., Bazylinski, D. A., and Schüler, D. (1998) Biomineralization of magnetic iron minerals in magnetotactic bacteria. Supramol. Sci. 5, 383-390.

Friedmann, E. I. and Ocampo-Friedmann, R. (1995) A primitive cyanobacterium as pioneer microorganism for terraforming Mars. Adv. Space Res. 3, 243-246.

Friedmann, E. I., Hua, M., and Ocampo-Friedmann, R. (1993) Terraforming Mars: dissolution of carbonate rocks by cyanobacteria. JBIS 46, 291-292.

Fukumori, Y., Oynagi, H., Yoshimatsu, K., Noguchi, Y., and Fujiwara, T. (1997) Enzymatic iron oxidation and reduction in magnetite synthesizing Magnetospirillum magnetotacticum. J. Phys. IV 7, 659-666.

Gerstell, M. F., Francisco, J. S., Yung, Y. L., Boxe, C., and Aaltonee E. T. (2001) Keeping Mars warm with new super greenhouse gases. Proc. Natl. Acad. Sci. USA 98, 2154-2157.

Gorby, Y. A., Beveridge, T. J., and Blakemore, R. P. (1988) Characterization of the bacterial magneto-some membrane. J. Bacteriol. 170, 834-841.

Grünberg, K., Müller, E. C., Otto, A., Reszka, R., Linder, D., Kube, M., Reinhardt, R., and Schüler, D. (2004) Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Appl. Environ. Microbiol. 70, 1040-1050.

Guerin, W. F. and Blakemore, R. P. (1992) Redox cycling of iron supports growth and magnetite synthesis by Aquaspirillum magnetotacticum. Appl. Environ. Microbiol. 58, 1102-1109.

Hancox, C. R. (1999) Terraformation of Mars. In: R. M. Zubrin and M. Zubrin (eds.) Proceedings of the Founding Convention of the Mars Society, Part III. Univelt Publisher, San Diego, CA, pp. 905-935.

Haynes, R. H. and McKay, C. P. (1992) The implantation of life on mars: feasibility and motivation. Adv. Space Res. 12, 133-140.

Heyen, U. and Schüler, D. (2003) Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl. Microbiol. Biotechnol. 61, 536-544.

Hiscox, J. A. (2000a) Biology and the Planetary Engineering of Mars. In: K. R. McMillen (ed.) The Case for Mars VI. Univelt Publisher, San Diego, CA, pp. 453-481.

Hiscox, J. A. (2000b) Selecting pioneer microorganisms for Mars. In: K. R. McMillen (ed.) The Case for Mars VI. Univelt, San Diego, CA, pp. 491-503.

Hiscox, J. A. and Thomas, D. J. (1995) Modification and selection of microorganisms for growth on Mars. J. Brit. Inter. Soc. 48, 419-426.

Jukes, H. (1991) Mars as a new abode for microbial life. J. Molec. Evol. 32, 355-357.

Kasama, T., Posfai, M., Chong, R. K. K., Finlayson, A. P., Buseck, P. R., Frankel, R. B., and Dunin-Borkowski, R. E. (2006) Magnetic properties, microstructure, composition, and morphology of greigite nanocrystals in magnetotactic bacteria from electron holography and tomography. Am. Mineral. 91, 1216-1229.

Keim, C. N., Abreu, F., Lins, U., Lins de Barros, H., and Farina, M. (2004) Cell organization and ultrastructure of a magnetotactic multicellular organism. J. Struct. Biol. 145, 254-262.

Lins, U., Keim, C. N., Evans, F. F., Farina, M., and Buseck, P. R. (2007) Magnetite (Fe3O4) and greigite (Fe3S4) crystals in magnetotactic multicellular organisms. Geomicrobiol. J. 24, 43-50.

Mann, S., Sparks, N. H. C., and Board, R. G. (1990) Magnetotactic bacteria: microbiology, biomineralization, palaeomagnetism and biotechnology. Adv. Microbiol. Physiol. 31, 125-181.

Marinova, M. M., McKay C. P., and Hashimoto, H. (2000) Warming Mars using artificial super-greenhouse gases. JBIS 53, 235-240.

Matsunaga, T., Tsujimura, N., Okamura, H., and Takeyama, H. (2000) Cloning and characterization of a gene, mpsA, encoding a protein associated with intracellular magnetic particles from Magnetospirillum sp. strain AMB-1. Biochem. Biophy. Res. Commun. 268, 932-937.

McKay, C. P. and Marinova, M. M. (2001) The Physics, Biology and Environmental Ethics of making Mars habitable. Astrobiology 1, 89-109.

McKay, C. P., Toon, O. B., and Kasting, J. F. (1991) Making Mars habitable. Nature 352, 489-496.

McKay, C. P., Friedman, E. I., Frankel, R. B., and Bazylinski, D. A. (2003) Magnetotactic bacteria on Earth and on Mars. Astrobiology 2, 263-270.

Moench, T. T. and Konetzka, W. A. (1978) A novel method for the isolation and study of a magneto-tactic bacterium. Arch. Microbiol. 119, 203-212.

Moisescu, C., Dumitru, L., and Ardelean, I. (2005) The growth of the magnetotactic bacterium Magnetospirillum gryphiswaldense under microaerobic conditions. Proceedings of the Institute of Biology of the Romanian Academy 7, 207-210.

Murray, J., Codispoti, L., and Friedrich, G. (1995) Oxidation-reduction environments: the suboxic zone in Black Sea. In: C. P. Huang, C. R. O'Melia and J. J. Morgan (eds.) Aquatic Chemistry, vol. 244. American Chemical Society, Washington, DC, pp. 157-176.

Nienow, J. A., McKay, C. P., and Friedmann, E. I. (1988) The cryptoendolithic microbial environment in the Ross Desert of Antarctica: light in the photosynthetically active region. Microb. Ecol. 16, 271-289.

Nussinov, M. D., Lysenko, S. V., and Patrikeev, V. V. (1994) Terraforming of Mars through terrestrial microorganisms and nanotechnological devices. J. Brit. Interplanet. Soc. 47, 319-320.

Petermann, H. and Bleil, U. (1993) Detection of live magnetotactic bacteria in South-Atlantic deep-sea sediments. Earth Planet. Sci. Lett. 117, 223-228.

Petersen, N., Weiss, D. G., and Vali, H. (1989) Magnetic bacteria in lake sediments. In: F. J. Lowes, D. W. Collinson, J. H. Parry, S. K. Runcorn, T. D. C., and A. Soward (eds.) Geomagnetism and Paleomagnetism. Kluwer, Dordrecht, pp. 231-241.

Popoviciu, D. R. (2006) Some Ideas Regarding the Biological Colonization of Planet Mars. http:// www.redcolony.com

Rodgers, F., Blakemore, R. P., Frankel, R. B., Bazylinski, D., Maratea, D., and Rodgers, C. (1990) Intercellular junctions, motility and magnetosome structure in a multicellular magnetotactic prokaryote. In: R. B. Frankel and R. B. Blakemore (eds.) Iron Biominerals. Plenum, New York, pp. 231-238.

Sagan, C. (1961) The planet Venus. Science 133, 849-858.

Sagan, C. (1973) Planetary engineering on Mars. Icarus 20, 513-514.

Schübbe, S., Kube, M., Scheffel, A., Wawer, C., Heyen, U., Meyerdierks, A., Madkour, M., Mayer, F., Reinhardt, R., and Schüler, D. (2003) Characterization on a spontaneous nonmagnetic mutant of Magnetospirillum gryphiswaldense reveals a large deletion comprising a putative magnetosome island. J. Bacteriol. 185, 5779-5790.

Schüler, D. (2004) Molecular analysis of a subcellular compartment: the magnetosome membrane in Magnetospirillum gryphiswaldense. Arch. Microbiol. 181, 1-7.

Schüler, D. and Baeuerlein, E. (1998) Dynamics of iron uptake and Fe3O4 biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J. Bacteriol. 180, 159-162.

Schüler, D. and Frankel, R. B. (1999) Bacterial magnetosomes: microbiology, biomineralization and biotechnological applications. Appl. Microbiol. Biotechnol. 52, 464-473.

Short, K. A. and Blakemore, R. P. (1986) Iron respiration-driven proton translocation in aerobic bacteria. J. Bacteriol. 167, 729-731.

Smith, M. J., Sheehan, P. E., Perry, L. L., O'Connor, K., Csonka, L. N., Applegate, B. M., and Whitman, L. J. (2006) Quantifying the magnetic advantage in magnetotaxis. Biophys. J. 91, 1098-1107.

Spring, S., Amann, R., Ludwig, W., Schleifer, K. H., Van Gemerden, H., and Petersen, N. (1993) Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl. Environ. Microbiol. 59, 2397- 2403.

Stephens, C. (2006) Bacterial cell biology: managing magnetosomes. Curr. Biol. 16, R363-R365.

Stolz, J. F. (1992) Magnetotactic bacteria: biomineralization, ecology, sediment magnetism, environmental indicator. In: H. C. W. Skinner (ed.) Biomineralization: Processes of Iron and Manganese; Modern and Ancient Environments. Catena-Verlag, Cremlingen-Destedt, pp. 133-145.

Stolz, J. F. (1993) Magnetosomes. J. Gen. Microbiol. 139, 1663-1670.

Tamegai, H., Yamanaka, T., and Fukumori, Y. (1993) Purification and properties of a 'cytochrom a01'-like hemoprotein from a magnetotactic bacterium, Aquaspirillummagnetotacticum. Biochim. Biophys. Acta. 1158, 137-243.

Tanaka, M., Okamura, Y., Arakaki, A., Tanaka, T., Takeyama, H., and Matsunaga, T. (2006) Origin of magnetosome membrane: proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics 6, 5234-5247.

Taylor, A. P., Barry, J. C., and Webb, R. I. (2001) Structural and morphological anomalies in magne-tosomes: possible biogenic origin for magnetite in ALH84001. J. Microscopy 201, 84-106.

Thomas-Keprta, K. L., Clemett, S. J., Bazylinski, D. A., Kirschvink, J. L., McKay, D. S., Wentworth, S. J., Vali, H., Gibson, E. K., Jr., and Romanek, C. S. (2002) Magnetofossils from ancient Mars: a robust biosignature in the Martian meteorite ALH84001. Appl. Environ. Microbiol. 68, 3663-3672.

Urban, J. E. (2000) Adverse effects of microgravity on the magnetotactic bacterium Magnetospirillum magnetotacticum. Acta Astronaut. 10, 775-780.

Weiss, B. P., Kim, S. S., Kirschvink, J. L., Kopp, R. E., Sankaran, M., Kobayashi, A., and Komeili, A. (2004) Magnetic tests for magnetosome chains in Martian meteorite ALH84001. Proc. Natl. Acad. Sci. USA 101, 8281-8284.

Williams, T. J., Zhang, C. L., Scott, J. H., and Bazylinski, D. A. (2006) Evidence for autotrophy via the reverse tricarboxylic acid cycle in the marine magnetotactic coccus strain MC-1. Appl. Environ. Microbiol. 72, 1322-1329.

Yamazaki, T., Oyanagi, H., Fujiwara, T., and Fukumori, Y. (1995) Nitrite reductase from the magne-totactic bacterium Magnetospirillum magnetotacticum - a novel cytochrome-cd(1) with Fe(II)-nitrite oxidoreductase activity. Eur. J. Biochem. 233, 665-671.

Zopfi, J. T., Ferdelman, T. G., Jorgensen, B. B., Teske, A., and Thamdrup, B. (2001) Influence of water column dynamics on sulfide oxidation and other major biogeochemical processes in the chemo-cline of Mariager Fjord (Denmark). Mar. Chem. 74, 29-51.

Zubrin, R. and Wagner, R. (ed.) (1996) The Case for Mars: The Plan to Settle the Red Planet and Why We Must. Free Press, New York.

Zubrin, R. M. and McKay, C. P. (1997) Technological requirements for terraforming Mars. JBIS 50, 83-92.

Mars Global Surveyor - Magnetic Field Experiment. http://mgs-mager.gsfc.nasa.gov

Terrestrial Magnetism. http://denali.gsfc.nasa.gov/terr_mag/index.html

Biodata of Charles H. Lineweaver, author of "Paleontological Tests: Human-Like Intelligence Is Not a Convergent Feature of Evolution"

Dr. Charles H. Lineweaver is currently an Associate Professor at the Planetary Science Institute in the Research School of Astronomy and Astrophysics and the Research School of Earth Sciences at the Australian National University, Canberra, Australia. He obtained his Ph.D. from the University of California at Berkeley in 1994 and continued his studies and research at Strasbourg Observatory and the University of New South Wales. Dr. Lineweaver's scientific interests are in the areas of: planetology, cosmology and astrobiology.

E-mail: [email protected]

Dr. Charles H. Lineweaver
0 0

Post a comment