Iron-Tolerant Cyanobacteria

Implications for Astrobiology
  • Igor Brown
  • Carlton Allen
  • Daniel L. Mummey
  • Svetlana Sarkisova
  • David S. McKay
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 11)

Iron is the fourth most abundant element in the Earth’s crust and the most abundant element in the Earth as a whole (Ehrilch, 2002). General agreement is that life evolved in the presence of soluble iron concentrations much greater than those typical today (MacLeod et al., 1994; Emerson and Moyer, 2002) and that life is based, therefore, on redox processes mediated by iron compounds (Beinert et al., 1997).

The importance of cyanobacteria (CB) to the geophysical evolution of life on Earth cannot be overstated. In addition to contributions to Earth’s biomass and poikilotrophy (Levit et al., 1999), cyanobacterial phototrophic activity from the Archean to present times is thought to have contributed significantly to presentday oxygen and carbon dioxide concentrations of our atmosphere (ibid.), thus driving the evolution of modern oxygen-dependent organisms. Even though the evolutionary path of oxygenic photosynthesis is well studied (Xiong et al., 2000; Xiong and Bauer, 2002; Olson and Blankenship, 2004; Iverson, 2006), what triggered the transition from anoxygenic to oxygenic photosynthesis is still not clear. The answer to this question might be obtained by the search for coincidences between the remarkable events in Earth and life’s evolution.


Band Iron Formation Oxygenic Photosynthesis Martian Atmosphere Anoxygenic Phototroph Martian Soil 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Allen, C.C., Probst, L.W., Flood, B.E., Longazo, T.G., Schelble, R.T., and Westall, F. (2004). Meridiani Planum hematite deposit and the search for evidence of life on Mars - iron mineral-ization of microorganisms in rock varnish. Icarus 171: 20-30.CrossRefGoogle Scholar
  2. Amaral Zettler, L.A., Gomez, F., Zettler, E., Keenan, B.G., Amils, R., and Sogin, M.L. (2002). Microbiology: eukaryotic diversity in Spain’s River of Fire. Nature 417: 137.CrossRefPubMedGoogle Scholar
  3. Amaral Zettler, L.A., Messerli, M.A., Laatsch, A.D., Smith, P.J.S., and Sogin, M.L. (2003). From genes to genomes: beyond biodiversity in Spain’s Rio Tinto. Biol. Bull. 204: 205-209.CrossRefPubMedGoogle Scholar
  4. Ananyev, G.M., Zaltsman, L., Vasko, C., and Dismikes, G.C. (2001). The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim. Biophys. Acta 1503: 52-68.CrossRefPubMedGoogle Scholar
  5. Beinert, H., Holm, R., and Munck, E. (1997). Iron-sulfur clusters: nature’s modular, multipurpose structures. Science 277: 653-659.CrossRefPubMedGoogle Scholar
  6. Belkin, S. and Padan, E. (1978). Hydrogen metabolism in the facultative anoxygenic cyanobacteria (blue-green algae): Oscillatoria limnetica and Aphanothece halophytica. Arch Microbiol. 23: 109-111.CrossRefGoogle Scholar
  7. Benderliev, K. (1999). Algae and cyanobacteria release organic chelators in the presence of inorganic Fe(III) thus keeping iron dissolved. Bulg. J. Plant Physiol. 25: 65-75.Google Scholar
  8. Benesova, J., Nickova, K., Ferimazova, N., and Stys, D. (2000). Morphological and physiological dif-ferences in Synechococcus elongatus during continuous cultivation at high iron, low iron, and iron deficient medium. Photosynthetica 38: 233-241.CrossRefGoogle Scholar
  9. Beukes, N. (2004). Biogeochemistry: early options in photosynthesis. Nature 431: 522-523.CrossRefPubMedGoogle Scholar
  10. Bibring, J.P., Langevin, Y., Mustard, J.F., et al. (2006). Global mineralogical and aqueous mars his-tory derived from OMEGA/Mars Express data. Science 312: 400-404.CrossRefPubMedGoogle Scholar
  11. Bishop, J.L., Rothshild, L.J., and Rogoff, D. (2006a). Nanophase iron oxides for ancient photosyn-thetic microbes. Astrobiology 6: 232-233.Google Scholar
  12. Bishop, J.L., Louris, S.K., Rogoff, D.A., and Rothschild, L.J. (2006b). Nanophase iron oxides as a key ultraviolet sunscreen for ancient photosynthetic microbes. Intern. J. Astrobiol. 5: 1-12.CrossRefGoogle Scholar
  13. Blank, C.E. (2004). Evolutionary timing of the origins of mesophilic sulfate reduction and oxygenic photosynthesis: A phylogenomic approach. Geobiology 2: 1-20.CrossRefGoogle Scholar
  14. Blankenship, R.E. and Hartman, H. (1998). Theorigin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23: 94-97.Google Scholar
  15. Boyer, G.L., Gillam, A.H., and Trick, C. (1987). Iron chelation and uptake, in: P. Fay, and C. van Baalen (eds.) The Cyanobacteria. Elsevier, Amsterdam, Netherlands, pp. 415-436.Google Scholar
  16. Braun, V., Hantke, K., and Koster, W. (1998). Bacterial iron transport: mechanisms, genetics, and reg-ulation. Met. Ions Biol. Syst. 35: 67-145.PubMedGoogle Scholar
  17. Brock, T.D. (1973). Lower pH limit for the existence of blue-green algae: evolutionary and ecological implications. Science 179: 480-483.CrossRefPubMedGoogle Scholar
  18. Brock, T.D. (1978). Thermophilic Microorganisms and Life at High Temperatures. Springer-Verlag, New York.Google Scholar
  19. Brown, I.I. (1994). Is Ca2+ the third coupling ion? Biochemistry (Moscow) 59: 1321-1323.Google Scholar
  20. Brown, I.I., Mummey, D., and Cooksey, K.E. (2005a). A novel cyanobacterium exhibiting an elevated tolerance for iron. FEMS Microbiol Ecol. 52: 307-314.CrossRefPubMedGoogle Scholar
  21. Brown, I.I., Mummey, D.L., and McKay, D.S. (2005b). Chroogloeocystis siderophila - a potential model for cyanobacteria-mediated Precambrian iron transformations. Astrobiology 5: 290.Google Scholar
  22. Brown, I.I., Mummey, D.L., Hinman, N., Schwandt, C., Garrison, G., Galindo, C., and McKay, D.S. (2005c). Molecular and biogeochemical characteristic of iron-tolerant cyanobacteria (IT CB) as potential tools for biogeochemistry, paleo-and exobiology. Proceedings of the International Symposium on Biogeochemistry. Jackson Hole.Google Scholar
  23. Brown, I.I., Mummey,.D.L., Lindsey, J., and McKay, D.S. (2005d). Iron-tolerant cyanobacteria: eco-physiology and fingerprinting. Proceedings of the 6th European Workshop on the Molecular Biology of Cyanobacteria. Gdansk, Poland.Google Scholar
  24. Brown, I.I, Mummey, D., Sarkisova S., Allen, C.C., and McKay, D.S. (2006a) Iron-tolerant cyanobac-teria as an effective tool to study early evolution of life and the development of biosignatures. Proceedings of the XXXVII Lunar and Planetary Sciences Conf.Google Scholar
  25. Brown, I., Jones J.P., Sternberg P., Bayless, D., Sarkisova, S., and McKay, D.S. (2006b). Iron-tolerant cyanobacteria for human habitation beyond Earth. Astrobiology 6: 177.Google Scholar
  26. Brown, I.I., Mummey, D., Sarkisova, S., Lindsay, J., Shen, J., Bryant, D., and McKay, D.S. (2006c) Siderophilic cyanobacteria: implications for Early Earth. Proceedings of the 12th International Symposium on Phototrophic Prokaryotes. France, 2006.Google Scholar
  27. Canfield, D.E. and Des Marais, D.J. (1993). Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim. Cosmochim. Acta 57: 3971-3984.CrossRefPubMedGoogle Scholar
  28. Catling, D.C.(2006). Atmospheric evolution of Mars, in: V. Gornitz(eds.) Encyclopedia of Paleoclimatology and Ancient Environments, Springer, New York.Google Scholar
  29. Cloud, P. (1973). Paleoecological significance of banded iron-formation. Econ. Geol. 68: 1135-1143.CrossRefGoogle Scholar
  30. Cockell, C.S. and Raven, J.A. (2004). Zones of photosynthetic potential on Mars and the early Earth. Icarus 169: 300-310.CrossRefGoogle Scholar
  31. Cohen, Y. (1984). Oxygenic photosynthesis, anoxygenic photosynthesis, and sulfate reduction in cyanobacterial mats, in: M.J. Klug and C.A. Reddy (eds.) Current Perspectives in Microbial Ecology. American Society of Microbiology, Washington D.C., pp. 435-441.Google Scholar
  32. Cohen, Y. (1989). Photosynthesis in cyanobacterial mats and its relation to the sulfur cycle: a model for microbial sulfur interactions, in: Y. Cohen and E. Rosenburg (eds.) Microbial Mats: Physiological Ecology of Benthic Microbial Communities. American Society for Microbiology, Washington D.C., pp. 22-36.Google Scholar
  33. Cohen, Y., Padan, E. and Shilo, M. (1975). Facultative anoxygenic photosynthesis in the cyanobac-terium Oscillatoria limnetica. J. Bacteriol. 123: 855-861.PubMedGoogle Scholar
  34. Croal, L.R., Gralnick, J.A., Malasarn, D., and Newman, D.K. (2004) The genetics of geochemistry. Annu. Rev. Genet. 38: 175-202.CrossRefPubMedGoogle Scholar
  35. Davies, G. F. (1995). Punctuated tectonic evolution of the Earth, Earth Planet Sci. Lett. 136: 363-379.Google Scholar
  36. Dismukes, G.C., Klimov, V.V., Baranov, S.V., Kozlov, Y.N., DasGupta, J., and Tyryshkin, A. (2001). The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc. Natl. Acad. Sci. U S A 98: 2170-2175.CrossRefPubMedGoogle Scholar
  37. Dobbin, P.S., Warren, L.H., Cook, N.J., McEwan, A.G., Powell, A.K., and Richardson, D.J. (1996). Dissimilatory iron(III) reduction by Rhodobacter capsulatus. Microbiology 142: 765-774.CrossRefGoogle Scholar
  38. Ehrenreich, A. and Widdel, F. (1994). Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl. Environ. Microbiol. 60: 4517-4526.PubMedGoogle Scholar
  39. Ehrilch, H.L. (2002). Geomicrobiology, Marcel Dekker, Inc., NY - Basel, pp. 345-428.Google Scholar
  40. Emerson, D. and Moyer, C. L. (2002). Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl. Environ. Microbiol. 68: 3085-3093.CrossRefPubMedGoogle Scholar
  41. Fairen, A.G., Fernandez-Remolar, D., Dohm, J.M., Baker, V.R., and Amils, R. (2004). Inhibition of carbonate synthesis in acidic oceans on early Mars. Nature 431: 423-426.CrossRefPubMedGoogle Scholar
  42. Ferris, M.J., Sheehan, K.B., Kuhl, M., Cooksey, K., Wigglesworth-Cooksey, B., Harvey, R., and Henson, J.M. (2005). Algal species and light microenvironment in a low-pH, geothermal micro-bial mat community. Appl. Environ. Microbiol. 71: 7164-7171.CrossRefPubMedGoogle Scholar
  43. Ghosh, D., Bal, B., Kashyap, V.K., and Pal, S. (2003). Molecular phylogenetic exploration of bacteria diversity in a Bakreshwar (India) hot spring and culture of Shewanella-related thermophiles. Appl. Environ. Microbiol. 69: 4332-4336.CrossRefPubMedGoogle Scholar
  44. Gress, C.D., Treble, R.G., Matz, C.J., and Weger, H.G. (2004). Biological availability of iron to the freshwater cyanobacterium Anabaena flos-aque. J. Phycol. 40: 879-886.CrossRefGoogle Scholar
  45. Gross, E.D. and Martin, D.F. (1996). Iron dependence of Lyngbya majuscula. J. Aquat. Plant Manag. 34: 17-20.Google Scholar
  46. Horvath, A., Pocs, T., Ganti, T., Berczi, Sz., and Szathmary, E. (2004). On the possibility of acrypto-biotic crust on Mars based on Northern and Southern ringed polar dune spots. Proceedings of the Lunar and Planetary Science Conference XXXV. Abstract 1914.Google Scholar
  47. Iverson, T.M. (2006). Evolution and unique bioenergetic mechanisms in oxygenic photosynthesis. Curr. Opin. Chem. Biol. 10: 91-100.CrossRefPubMedGoogle Scholar
  48. Kappler, A., Pasquero, C., Konhauser, K.O., and Newman, D.K. (2005). Deposition of Banded Iron Formations by photoautotrophic Fe(II)-oxidizing bacteria. Geology 33: 865-868.CrossRefGoogle Scholar
  49. Konhauser, K.O. (2004). The role of bacteria in banded iron formations. Conference Proceedings of the 11th International Symposium on Water-Rock Interactions. Saratoga Springs, New York.Google Scholar
  50. Konhauser K.O., Hamade T., Morris R.C., Ferris F.G., Southam G., Raiswell R., and Canfield, D. (2002) Did bacteria form Precambrian banded iron formations? Geology 30: 1079-1082.CrossRefGoogle Scholar
  51. Konhauser, K.O., Newman, D.K., and Kappler, A. (2005). The potential significance of microbial Fe(III) reduction during deposition of precambrian Banded Iron Formations. Geobiology 3: 167-177.CrossRefGoogle Scholar
  52. Kump, L. (2005). Ocean science: Ironing out biosphere oxidation. Science 307: 1058-1059.CrossRefPubMedGoogle Scholar
  53. Levit, G.S., Gorbushina, A.A., and Krumbein, W.E. (1999). Geophysiology and parahistology of ben-thic microbial mats with special reference to the dissymmetry principle of Pasteur-Curie-Vernadskij. Bulletin de l’Institut Oceanographique, Monaco, special issue, 19: 175-196.Google Scholar
  54. Lindsay, J.F. and Brasier, M.D. (2002a). Did global tectonics drive early biosphere evolution? Carbon isotope record from 2.6 to 1.9 Ga carbonates of Western Australian basins. Precambrian Res. 114: 1-34.CrossRefGoogle Scholar
  55. Lindsay, J.F. and Brasier, M.D. (2002b). A comment on tectonics and the future of terrestrial life -reply. Precambrian Res. 118: 293-295.CrossRefGoogle Scholar
  56. Lindsay, J.F. and Brasier, M.D. (2004). The evolution of the Precambrian atmosphere: carbon isotopic evidence from the Australian continent, in: P.G. Eriksson, W. Altmann, D.R. Nelson, W.U. Mueller, and O. Catuneau, (eds.) The Precambrian Earth: Tempos and Events. Elsevier, pp. 388-403.Google Scholar
  57. Little, B.J., Wagner, P.A., and Lewandowski, Z. (1997). Spatial relationships between bacteria and mineral surfaces. Rev. Mineral 35:123-159.Google Scholar
  58. MacLeod, G., McKeown, C., Hall, A. J., and Russell, M. J. (1994). Hydrothermal and oceanic pH conditions of possible relevance to the origin of life. Orig. Life. Evol. Biosph. 24: 19-41.CrossRefPubMedGoogle Scholar
  59. Navarro-Gonzalez, R., Navarro K.F., de la Rosa, J., Iniguez E., Molina, P., Miranda L.D., Morales, P., Cienfuegos, E., Coll, P., Raulin, F., Amils, R., and McKay, C.P. (2006) The limitations on organic detection in Mars-like soils by thermal volatilization-gas chromatography-MS and their implications for the Viking results. Proc. Natl. Acad. Sci. U S A 103: 16089-16094.CrossRefPubMedGoogle Scholar
  60. Olson, J.M. (2001). Evolution of Photosynthesis’ (1970), re-examined thirty years later. Photosynth. Res. 68: 95-112.CrossRefPubMedGoogle Scholar
  61. Olson, J.M. (2006). Photosynthesis in the Archean Era. Photosynth. Res. 2: 1-9.Google Scholar
  62. Olson, J.M. and Blankenship, R.E. (2004). Thinking about the evolution of photosynthesis. Photosynth. Res. 80:373-386.CrossRefPubMedGoogle Scholar
  63. Paczuska, L. and Kosakowska, A. (2003). Is irona limiting factor of Nodularia spumigena blooms? Oceanologia 45: 679-692.Google Scholar
  64. Parenteau, M.N., Embaye, T., Jahnke, L.L., and Cady, S.L. (2003). Microbial Biosignatures in high iron thermal springs. Proceedings of the American Geophysical Union, Fall Meeting 2003. Abstract #B12B-0778.Google Scholar
  65. Parenteau, M.N., Jahnke, L.L., Embaye, T., and Cady S.L. (2005) Biosignature formation by cyanobacteria and Chloroflexus in the shellow deposits of a high iron thermal spring. Astrobiology 5: 291.Google Scholar
  66. Pierson, B.K. and Olson, J.M. (1989). Evolution of photosyntheses in anoxygenic photosynthentic prokaryotes, in: Y. Cohen and E. Rosenberg (eds.) Microbial Mats, Physiological Ecology of Benthic Communities. American Society of Microbiology, Washington D.C., pp 402-427.Google Scholar
  67. Pierson, B.K. and Parenteau, M.N. (2000). Phototrophs in high iron microbial mats: microstructure of mats in iron-depositing hot springs. FEMS Microbiol. Ecol. 32: 181-196.CrossRefPubMedGoogle Scholar
  68. Pierson, B.K., Parenteau, M.N., and Griffin, B.M. (1999). Phototrophs in high-iron-concentration microbial mats: physiological ecology of phototrophs in an iron-depositing hot spring. Appl. Environ. Microbiol. 65: 5474-5483.PubMedGoogle Scholar
  69. Rouxel, O.J., Bekker, A., and Edwards, K.J. (2005). Iron isotope constraints on the Archean and Paleoproterozoic ocean redox state. Science 307: 1088-1091.CrossRefPubMedGoogle Scholar
  70. Sanchez-Baracaldo, P., Hayes, P.K., and Blank, C.E. (2005). Evolution of morphological and habitat characters in the Cyanobacteria using a compartmentalization approach. Geobiology 3: 145-165.CrossRefGoogle Scholar
  71. Stal, L.J. (2000). Cyanobacterial Mats and Stromatolites, in: B.A. Whitton and M. Potts (eds.) The Ecology of Cyanobacteria - Their Diversity in Time and Space. Kluwer Academic Publisher, pp. 61-120.Google Scholar
  72. Swingley, W.D., Hohmann-Marriott, M.F., Le Olson, T., and Blankenship, R.E. (2005). Effect of iron on growth and ultrastructure of Acaryochloris marina. Appl. Environ. Microbiol. 71: 8606-8610.CrossRefPubMedGoogle Scholar
  73. Tomitani, A., Knoll, A.H., Cavanaugh, C.M., and Ohno, T. (2006). The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc. Natl. Acad. Sci. U S A 103: 5442-5447.CrossRefPubMedGoogle Scholar
  74. Trouwborst, R., Koch, G., Druschel, G., Shanks, L., Luther G.W., and Pierson, B. (2004). Hot Spring Microbial Mats: A Model for Precambrian Banded Iron Formations? Proceedings of the AbSciCon (NASA Astrobiology Science Conference). Ames Research Center.Google Scholar
  75. Wentworth, S.J., Gibson, E.K., Velbel, M.A., and McKay, D.S. (2005) Antarctic Dry Valleys and indigenous weathering in Mars meteorites: implications for water and life on Mars. Icarus, v. 174, pp. 382-395.CrossRefGoogle Scholar
  76. Widdel, F., Schnell, S., Heising, S., Ehrenreich, A., Assmus, B., and Schink, B. (1993). Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362: 834-836.CrossRefGoogle Scholar
  77. Wilson, C.I., Hinman, N.W., and Sheridan, R.P. (2000). Hydrogen peroxide formation and decay in iron-rich geothermal waters: the relative roles of abiotic and biotic mechanisms. Photochemistry and photobiology 71: 691-699.CrossRefPubMedGoogle Scholar
  78. Xiong, J. and Bauer, C.E. (2002). Complex evolution of photosynthesis. Annu. Rev. Plant Biol. 53: 503-521.CrossRefPubMedGoogle Scholar
  79. Xiong, J., Fischer, W.M., Inoue K., Nakahara, M., and Bauer, CE. (2000). Molecular evidence for the early evolution of photosynthesis. Science 289: 1.CrossRefGoogle Scholar
  80. Zavarzin, G.A. (1993) Epicontinental soda lakesas the possible relict biotopes of terrestrial biota formation. Mikrobiologiya 62: 789-800.Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Igor Brown
    • 1
  • Carlton Allen
    • 1
  • Daniel L. Mummey
    • 2
  • Svetlana Sarkisova
    • 1
  • David S. McKay
    • 1
  1. 1.National Aeronautics and Space Administration Johnson Space CenterHoustonUSA
  2. 2.Division of Biological SciencesUniversity of MontanaMissoulaUSA

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