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Manganese carbonates as possible biogenic relics in Archean settings

Published online by Cambridge University Press:  13 July 2016

Blanca Rincón-Tomás
Affiliation:
Georg-August-University Göttingen, Institute of Microbiology and Genetics, Grisebachstraße 8, 37077 Göttingen, Germany
Bahar Khonsari
Affiliation:
Georg-August-University Göttingen, Institute of Microbiology and Genetics, Grisebachstraße 8, 37077 Göttingen, Germany
Dominik Mühlen
Affiliation:
Georg-August-University Göttingen, Institute of Microbiology and Genetics, Grisebachstraße 8, 37077 Göttingen, Germany
Christian Wickbold
Affiliation:
Georg-August-University Göttingen, Institute of Microbiology and Genetics, Grisebachstraße 8, 37077 Göttingen, Germany
Nadine Schäfer
Affiliation:
Georg-August-University Göttingen, Göttingen Centre of Geosciences, Goldschmidtstraße 3, 37077 Göttingen,Germany
Dorothea Hause-Reitner
Affiliation:
Georg-August-University Göttingen, Göttingen Centre of Geosciences, Goldschmidtstraße 3, 37077 Göttingen,Germany
Michael Hoppert*
Affiliation:
Georg-August-University Göttingen, Institute of Microbiology and Genetics, Grisebachstraße 8, 37077 Göttingen, Germany
Joachim Reitner
Affiliation:
Georg-August-University Göttingen, Göttingen Centre of Geosciences, Goldschmidtstraße 3, 37077 Göttingen,Germany Göttingen Academy of Sciences and Humanities, Theaterstraße 7, 37073 Göttingen, Germany

Abstract

Carbonate minerals such as dolomite, kutnahorite or rhodochrosite are frequently, but not exclusively generated by microbial processes. In recent anoxic sediments, Mn(II)carbonate minerals (e.g. rhodochrosite, kutnahorite) derive mainly from the reduction of Mn(IV) compounds by anaerobic respiration. The formation of huge manganese-rich (carbonate) deposits requires effective manganese redox cycling in an oxygenated atmosphere. However, putative anaerobic pathways such as microbial nitrate-dependent manganese oxidation, anoxygenic photosynthesis and oxidation in ultraviolet light may facilitate manganese cycling even in an early Archean environment, without the availability of oxygen. In addition, manganese carbonates precipitate by microbially induced processes without change of the oxidation state, e.g. by pH shift. Hence, there are several ways how these minerals could have been formed biogenically and deposited in Precambrian sediments. We will summarize microbially induced manganese carbonate deposition in the presence and absence of atmospheric oxygen and we will make some considerations about the biogenic deposition of manganese carbonates in early Archean settings.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

Agrawal, A. & Grieg, L.M. (2013). In situ detection of anaerobic alkane metabolites in subsurface environments. Front. Microbiol. 4, 140. doi: 10.3389/fmicb.2013.00140.CrossRefGoogle ScholarPubMed
Anbar, A.D. & Knoll, A.H. (2002). Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 11371142.Google Scholar
Anbar, A.D. et al. (2007). A whiff of oxygen before the Great Oxidation event? Science 317, 19031906.CrossRefGoogle ScholarPubMed
Boogerd, F.C. & de Vrind, J.P. (1987). Manganese oxidation by Leptothrix discophora . J. Bacteriol. 169, 489494.Google Scholar
Bower, D.M., Steele, A., Fries, M.D. & Kater, L. (2013). Micro Raman spectroscopy of carbonaceous material in microfossils and meteorites: improving a method for life detection. Astrobiology 13, 103113.CrossRefGoogle ScholarPubMed
Brasier, M., Green, O., Lindsay, J., McLoughlin, N., Steele, A. & Stoakes, C. (2005). Critical testing of Earth's oldest putative fossil assemblage from the ca. 3.5Ga Apex chert, Chinaman Creek, Western Australia. Precambr. Res. 140, 55102.Google Scholar
Brouwers, G. (2000). Bacterial Mn2+ oxidizing systems and multicopper oxidases: an overview of mechanisms and functions. Geomicrobiol. J. 17, 124.Google Scholar
Burke, I.T. & Kemp, A.E.S. (2002). Microfabric analysis of Mn-carbonate laminae deposition and Mn-sulfide formation in the Gotland Deep, Baltic Sea. Geochim. Cosmochim. Acta 66, 15891600.CrossRefGoogle Scholar
Cabello, P., Roldán, M.D. & Moreno-Vivián, C. (2004). Nitrate reduction and the nitrogen cycle in archaea. Microbiology 150, 35273546.CrossRefGoogle ScholarPubMed
Caccavo, F., Blakemore, R.P. & Lovley, D.R. (1992). A hydrogen-oxidizing, Fe(III)-reducing microorganism from the Great Bay estuary, New Hampshire. Appl. Environ. Microbiol. 58, 32113216.CrossRefGoogle ScholarPubMed
Canfield, D.E. (1998). A new model for Proterozoic ocean chemistry. Nature 396, 450453.Google Scholar
Castresana, J. & Moreira, D. (1999). Respiratory chains in the last common ancestor of living organisms. J. Mol. Evol. 49, 453460.Google Scholar
Castresana, J., Lübben, M., Saraste, M. & Higgins, D.G. (1994). Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13, 25162525.Google Scholar
Corstjens, P.L.A.M., de Vrind, J.P.M., Westbroek, P. & de Vrind-de Jong, E.W. (1992). Enzymatic iron oxidation by Leptothrix discophora: identification of an iron oxidizing protein. Appl. Environ. Microbiol. 58, 450454.CrossRefGoogle ScholarPubMed
Crowe, S.A., Døssing, L.N., Beukes, N.J., Bau, M., Kruger, S.J., Frei, R. & Canfield, D.E. (2013). Atmospheric oxygenation three billion years ago. Nature 501, 535538.CrossRefGoogle ScholarPubMed
Downs, R.T. (2006). The RRUFF Project: an integrated study of the chemistry, crystallography, Raman and infrared spectroscopy of minerals. In Program and Abstracts of the 19th General Meeting of the Int. Mineralogical Association in Kobe, Japan. O03–13.Google Scholar
Duda, J.P., Van Kranendonk, M.J., Thiel, V., Ionescu, D., Strauss, H., Schäfer, N. & Reitner, J. (2016). A rare glimpse of paleoarchean life: geobiology of an exceptionally preserved microbial mat facies from the 3.4 Ga Strelley Pool Formation, Western Australia. PLoS ONE 11, e0147629. doi: 10.1371/journal.pone.0147629.CrossRefGoogle ScholarPubMed
Fan, D.L., Hein, J.R. & Ye, J. (1999). Ordovician reef-hosted Jiaodingshan Mn–Co deposit and Dawashan Mn deposit, Sichuan Province. Ore Geol. Rev. 15, 135151.Google Scholar
Fennel, K., Follows, M. & Falkowski, P.G. (2005). The co-evolution of the nitrogen, carbon and oxygen cycles in the Proteozoic ocean. Am. J. Sci. 305, 526545.Google Scholar
Fischer, F. & Tropsch, H. (1925). Über die direkte Synthese von Erdöl-Kohlenwasserstoffen bei gewöhnlichem Druck. (Erste Mitteilung). Berichte der deutschen chemischen Gesellschaft (A and B Series) 59, 830831.CrossRefGoogle Scholar
Fisher, W.W., Hemp, J. & Johnson, J.E. (2015). Manganese and the evolution of photosynthesis. Orig. Life Evol. Biosph. 45, 351357.Google Scholar
Glasby, G. (1984). Manganese in the marine environment. Oceanogr. Mar. Biol. Ann. Rev. 22, 195210.Google Scholar
Glasby, G. & Schulz, H.D. (1999). EH, pH diagrams for Mn, Fe, Co, Ni, Cu and As under seawater conditions: application of two new types of EH, pH diagrams to the study of specific problems in marine geochemistry. Aquat. Geochem. 5, 227248.Google Scholar
Glenn, J.K., Akileswaran, L. & Gold, M.H. (1986). Mn(II) oxidation is the principal function of the extracellular Mn peroxidase from Phanerochaete chrysosporium . Arch. Biochem. Biophys. 251, 688696.CrossRefGoogle ScholarPubMed
Godfrey, L.V. & Falkovski, G. (2009). The cycling and redox state of nitrogen in the Archaean ocean. Nat. Geosci. 2, 725729.Google Scholar
Golding, S.D., Duck, L.J., Young, E., Baublys, K.A., Glikson, M. & Kamber, B.S. (2011). Earliest seafloor hydrothermal systems on Earth: comparison with modern analogues. In Earliest Life on Earth: Habitats, Environments and Methods of Detection, ed. Golding, S.D. & Glikson, M., pp. 1550. Springer B.V., Dordrecht.CrossRefGoogle Scholar
González-Muñoz, M.T., De Linares, C., Martínez-Ruiz, F., Morcillo, F., Martín-Ramos, D. & Arias, J.M. (2008). Ca-Mg kutnahorite and struvite production by Idiomarina strains at modern seawater salinities. Chemosphere 72, 465472.CrossRefGoogle ScholarPubMed
Hallmann, C., Stannek, L., Fritzlar, D., Hause-Reitner, D., Friedl, T. & Hoppert, M. (2013). Molecular diversity of phototrophic biofilms on building stone. FEMS Microbiol. Ecol. 84, 355372.Google Scholar
Hashimoto, H., Yokoyama, S., Asaoka, H., Kusano, Y., Ikeda, Y., Seno, M., Takada, J., Fujii, T., Nakanishi, M. & Murakami, R. (2007). Characteristics of hollow microtubes consisting of amorphous iron oxide nanoparticles produced by iron oxidizing bacteria, Leptothrix ochracea . J. Magn. Magn. Mater. 310, 24052407.Google Scholar
Hoashi, M., Bevacqua, D.C., Otake, T., Watanabe, Y., Hickman, A.H., Utsunomiya, S. & Ohmoto, H. (2009). Primary haematite formation in an oxygenated sea 3.46 billion years ago. Nat. Geosci. 2, 301306.CrossRefGoogle Scholar
Hoppert, M. & Holzenburg, A. (1998). Electron Microscopy in Microbiology. Bios-Springer in Association with the Royal Microscopical Society, Oxford, UK.Google Scholar
Hou, S. et al. (2004). Genome sequence of the deep sea-proteobacterium Idiomarina loihiensis reveals amino acid fermentation as a source of carbon and energy. Proc. Natl. Acad. Sci. USA 101, 1803618041.CrossRefGoogle ScholarPubMed
Huber, R., Kristjanson, J.K. & Stetter, K.O. (1987). Pyrobaculum gen. nov., a new genus of neutrophil, rod-shaped archaeabacteria from continental solfataras growing optimally at 100°C. Arch. Microbiol. 149, 95101.Google Scholar
Huckriede, H. & Meischner, D. (1996). Origin and environment of manganese-rich sediments within black-shale basin. Geochim. Cosmochim. Acta 60, 13991413.Google Scholar
Hulth, S., Aller, R.C. & Gilbert, F. (1999). Coupled anoxic nitrification/manganese reduction in marine sediments. Geochim. Cosmochim. Acta 63, 4966.Google Scholar
Johnson, J.E., Webb, S.M., Thomas, K., Ono, S., Kirschvink, J.L. & Fischer, W.W. (2013). Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc. Natl. Acad. Sci. USA 110, 1123811243.CrossRefGoogle ScholarPubMed
Johnson, K.S. (1982). Solubility of rhodochrosite (MnCO3) in water and seawater. Geochim. Cosmochim. Acta 46, 18051809.Google Scholar
Kämper, M., Vetterkind, S., Berker, R. & Hoppert, M. (2004). Methods for in situ detection and characterization of extracellular polymers in biofilms by electron microscopy. J. Microbiol. Methods 57, 5564.Google Scholar
Kashefi, K. & Lovley, D.R. (2000). Reduction of Fe(III), Mn(IV) and toxic metals at 100°C by Pyrobaculum islandicum, Appl. Environ. Microbiol. 66, 10501056.CrossRefGoogle Scholar
Kasting, J.F. (1993). Earth's early atmosphere. Science 259, 920926.Google Scholar
Kokoschka, S., Dreier, A., Romoth, K., Taviani, M., Schäfer, N., Reitner, J. & Hoppert, M. (2015). Isolation of anaerobic bacteria from terrestrial mud volcanoes (Salse di Nirano, Northern Apennines, Italy). Geomicrobiol. J. 32, 355364.CrossRefGoogle Scholar
Konhauser, K. (2006). Introduction to Geomicrobiology. Wiley-Blackwell, New York.Google Scholar
Larue, D.K. (1981). The Chocolay Group, Lake Superior region, U.S.A.: sedimentologic evidence for deposition in basinal and platform settings on an early Proterozoic craton. Geol. Soc. Am. Bull. 92, 417435.Google Scholar
Li, C., Cheng, M., Algeo, T.J. & Xie, S. (2015). A theoretical prediction of chemical zonation in early oceans (>520 Ma). Sci. China Earth Sci. 58, 19011909.CrossRefGoogle Scholar
Li, W.Q., Czaja, A.D., Van Kranendonk, M.J., Beard, B.L., Roden, E.E. & Johnson, C.M. (2013). An anoxic, Fe(II)-rich, U-poor ocean 3.46 billion years ago. Geochim. Cosmochim. Acta 120, 6579.Google Scholar
Liaw, Y.P., Sisterson, D.L. & Miller, N.L. (1990). Comparison of field, laboratory, and theoretical estimates of global nitrogen fixation by lightning. J. Geophys. Res. 95, 2248922494.Google Scholar
Lindsay, J.F., Brasierb, M.D., McLoughlinb, N., Greenb, O.R., Fogelc, M., Steelec, A. & Mertzmand, S.A. (2005). The problem of deep carbon - an Archean paradox. Precambr. Res. 143, 122.CrossRefGoogle Scholar
Madison, A.S., Tebo, B.M., Mucci, A., Sundby, B. & Luther, G.W. (2013). Abundant porewater Mn(III) is a major component of the sedimentary redox system. Science 341, 875878.Google Scholar
Marshall, A.O., Emry, J.R. & Marshall, C.P. (2012). Multiple generations of carbon in the Apex Chert and implications for preservation of microfossils. Astrobiology 12, 160166.Google Scholar
Marshall, C.P., Love, G.D., Snape, C.E., Hill, A.C., Allwood, A.C., Walter, M.R., Van Kranendonk, M.J., Bowden, S.A., Sylva, S.P. & Summons, R.E. (2007). Structural characterization of kerogen in 3.4 Ga Archaean cherts from the Pilbara Craton, Western Australia. Precambr. Res. 155, 123.Google Scholar
Marshall, C.P., Edwards, H.G.M. & Jehlicka, J. (2010). Understanding the application of Raman spectroscopy to the detection of traces of life. Astrobiology 10, 229243.Google Scholar
McCollom, T.M. (2003). Formation of meteorite hydrocarbons from thermal decomposition of siderite (FeCO3). Geochim. Cosmochim. Acta 67, 311317.Google Scholar
McCollom, T.M. & Seewald, J.S. (2006). Carbon isotope composition of organic compounds produced by abiotic synthesis under hydrothermal conditions. Earth Planet. Sci. Lett. 243, 7484.Google Scholar
Meister, P., Bernasconi, S.M., Aiello, I.W., Vasconcelos, C. & McKenzie, J.A. (2009). Depth and controls of Ca-rhodochrosite precipitation in bioturbated sediments of the Eastern Equatorial Pacific, ODP Leg 201, Site 1226 and DSDP Leg 68, Site 503. Sedimentology 56, 15521568.Google Scholar
Mojzsis, A., Arrhenius, G., McKeegan, K.D., Harrison, T.M., Nutman, A.P. & Friend, C.R.L. (1996). Evidence for life on Earth before 3,800 million years ago. Nature 384, 5559.Google Scholar
Myers, C.R. & Nealson, K.H. (1988). Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240, 13191321.CrossRefGoogle ScholarPubMed
Myers, C.R. & Nealson, K.H. (1990). Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciens MR-1. J. Bacteriol. 172, 62326238.Google Scholar
Nealson, K.H. & Myers, C.R. (1992). Microbial reduction of manganese and iron: new approaches to carbon cycling. Appl. Environ. Microbiol. 58, 439443.Google Scholar
Nealson, K.H. & Saffarini, D. (1994). Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 48, 311–43.Google Scholar
Noffke, N., Christian, D., Wacey, D. & Hazen, R.M. (2013). Microbially induced sedimentary structures recording an ancient ecosystem in the ca. 3.48 billion-Year-Old Dresser Formation, Pilbara, Western Australia. Astrobiology 13, 11031124.Google Scholar
Okita, P.M., Maynard, J.B., Spikers, E.C. & Force, E.R. (1988). Isotopic evidence for organic matter oxidation by manganese reduction in the formation of stratiform manganese carbonate ore. Geochim. Cosmochim. Acta 52, 24792685.Google Scholar
Olson, S.L., Kump, L.R. & Kasting, J.F. (2013). Quantifying the areal extent and dissolved oxygen concentration of Archean oxygen oases. Chem. Geol. 362, 3543.Google Scholar
Pedersen, T.F. & Price, N.B. (1982). The geochemistry of manganese carbonate in Panama Basin sediments. Geochim. Cosmochim. Acta 46, 5968.Google Scholar
Planavsky, N.J. et al. (2014). Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat. Geosci. 7, 283286.Google Scholar
Riding, R., Fralick, P. & Liang, L. (2014). Identification of an Archaean marine oxygen oasis. Precambr. Res. 251, 232237.Google Scholar
Roden, E.R. & Lovley, D.R. (1993). Dissimilatory Fe(III) reduction by the marine microorganism Desulfuromonas acetoxidans . Appl. Environ. Microbiol. 59, 734742.Google Scholar
Roy, S. (1997). Genetic diversity of manganese deposition in the terrestrial geological record. Geol. Soc. Spec. Publ. 119, 527.Google Scholar
Sabivora, J.S., Cloetens, L.F.F., Vanhaecke, L., Forrez, I., Verstraete, W. & Boon, N. (2008). Manganese-oxidizing bacteria mediate the degradation of 17α-ethinylestradiol. Microbiol. Biotechnol. 1, 507512.Google Scholar
Saito, M.A., Sigman, M. & Morel, F.M.M. (2003). The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean/Proterozoic boundary? Inorg. Chim. Acta 356, 308318.Google Scholar
Schidlowski, M. (1988). 3,800-million-year isotopic record of life from carbon in sedimentary rocks. Nature 333, 313318.Google Scholar
Schmidt, C., Behrens, S. & Kappler, A. (2010). Ecosystem functioning from a geomicrobiological perspective – a conceptual framework for biogeochemical iron cycling. Environ. Chem. 7, 399405.Google Scholar
Spiro, T.G., Bargar, J.R., Sposito, G. & Tebo, B.M. (2010). Bacteriogenic manganese oxides. Acc. Chem. Res. 19, 29.Google Scholar
Suarez-Zuluaga, D.A., Weijma, J., Timmers, P.H. & Buisman, C.J. (2015). High rates of anaerobic oxidation of methane, ethane and propane coupled to thiosulphate reduction. Environ. Sci. Pollut. Res. Int. 22, 36973704.Google Scholar
Tebo, B.M., Bargar, J.R., Clement, B.G., Dick, G.J., Murray, K.J., Parker, D., Verity, R. & Webb, S.M. (2004). Biogenic manganese oxides: properties and mechanisms of formation. Annu. Rev. Earth Planet Sci. 32, 287328.CrossRefGoogle Scholar
Thompson, I.A., Huber, D.M., Guest, C.A. & Schulze, D.G. (2005). Fungal manganese oxidation in a reduced soil. Environ. Microbiol. 9, 14801487.Google Scholar
Tice, M.M. & Lowe, D.R. (2004). Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431, 549552.Google Scholar
Trouwborst, R.E., Clement, B.G., Tebo, B.M., Glazer, B.T. & Luther, G.W. (2006). Soluble Mn(III) in suboxic zones. Science 313, 19551957.Google Scholar
van Zuilen, M.A., Lepland, A. & Arrhenius, G. (2002). Reassessing the evidence for the earliest traces of life. Nature 418, 627630.Google Scholar
Zehnder, A.J.B. & Stumm, W. (1988). Geochemistry and biogeochemistry of anaerobic habitats. In: Biology of Anaerobic Microorganisms, ed. Zehnder, A.J.B., pp. 138. John Wiley & Sons, New York.Google Scholar
Zerkle, A., House, C.H. & Brantley, S.L. (2005). Biogeochemical signatures trough time as inferred from whole microbial genomes. Am. J. Sci. 305, 567–502.Google Scholar