Experimental Modeling of Bacterially-Induced Ca Carbonate Precipitation: New Insights on Possible Mechanisms

Abstract:

The contribution of microorganisms, particularly bacteria, in carbonate mineral formation, the main natural processes controlling CO₂ level in the atmosphere, has played an important role since the Archean Eon. In this study we review our recent experimental work on CaCO₃ precipitation induced by two anoxygenic phototrophic bacteria (APB), Rhodovulum steppense A-20s^T and Rhodovulum sp. S-17-65, and by cyanobacteria Gloeocapsa sp. f-6gl. These bacteria are representatives of two important groups of photosynthetic organisms present at the Earth surface both in the past and at the present times. The mechanisms of organomineralization deriving from APB and cyanobacteria activities are drastically different and relate to the main physical and chemical processes controlling CaCO₃ precipitation from aqueous solution, essentially local supersaturation with respect to carbonates induced by photosynthesis outside the living cells and Ca adsorption onto cell surface and the associated extracellular polymeric substances (EPS).The APB can physiologically control their surface potential to electrostatically attract nutrients at alkaline pH, while rejecting Ca ions to prevent Ca adsorption and subsequent CaCO₃ precipitation in the vicinity of cell surface and thus, cell incrustation. In contrast to other previously-investigated calcifying bacteria, no cellular protection mechanism against Ca²⁺ adsorption and subsequent carbonate precipitation has been evidenced for cyanobacteria Gloeocapsa sp. f-6gl. This is most likely linked to the peculiar cellular organization of this species that involves several cells clustered in one single capsule. In this regard, colony-forming, EPS-rich, capsular cyanobacteria may be among the most efficient calcifying microorganisms all along the Earth history and can be of interest for various technological applications involving carbonation.

• Periodical: Key Engineering Materials (Volume 672)
• Pages: 21-39
• DOI: https://doi.org/10.4028/www.scientific.net/KEM.672.21
• Online since: January 2016
• Authors: Irina A. Bundeleva, Liudmila S. Shirokova, Elena I. Kompantseva, Pascale Bénézeth, Bénédicte Ménez, Frédéric Marin, Oleg S. Pokrovsky
• Keywords: Anoxygenic Phototrophic Bacteria, Biomineralization, Carbonation Kinetics, Cyanobacteria, Gloeocapsa sp, Photosynthesis, Precipitation Mechanism, Rhodovulum sp, Zeta-Potential

References

[1] O.S. Pokrovsky, R.E. Martinez, S.V. Golubev, E.I. Kompantseva, L.S. Shirokova, Adsorption of metals and protons on Gloeocapsa sp. cyanobacteria: A surface speciation approach, Applied Geochemistry 23 (2008) 2574-2588.

DOI: 10.1016/j.apgeochem.2008.05.007

[2] I.A. Bundeleva, L.S. Shirokova, P. Bénézeth, O.S. Pokrovsky, E.I. Kompantseva, S. Balor, Zeta-potential of anoxygenic phototrophic bacteria and Ca adsorption at the cell surface: implications for cell protection from CaCO3 precipitation in alkaline solutions, Journal of Colloid and Interface Science 360 (2011).

DOI: 10.1016/j.jcis.2011.04.033

[3] I.A. Bundeleva, L.S. Shirokova, P. Bénézeth, O.S. Pokrovsky, E.I. Kompantseva, S. Balor, Calcium carbonate precipitation by anoxygenic phototrophic bacteria, Chemical Geology 291 (2012) 116-131.

DOI: 10.1016/j.chemgeo.2011.10.003

[4] I.A. Bundeleva, L.S. Shirokova, O.S. Pokrovsky, P. Bénézeth, B. Ménez, E. Gérard, S. Balor, Calcium carbonate precipitation by cyanobacteria Gloeocapsa sp., Chemical Geology 374 (2014) 44-60.

DOI: 10.1016/j.chemgeo.2014.03.007

[5] M. Dittrich, P. Kurz, B. Wehrli, The role of autotrophic picocyanobacteria in calcite precipitation in an oligotrophic lake, Geomicrobiology Journal 21 (2004) 45-53.

DOI: 10.1080/01490450490253455

[6] S Douglas, T.J. Beveridge, Mineral formation by bacteria in natural microbial communities, FEMS Microbiology Ecology 26 (1998) 79–88.

DOI: 10.1111/j.1574-6941.1998.tb00494.x

[7] N. Mozes, P.G. Rouxhet, Microbial hydrophobicity and fermentation technology. In: Doyle, R.J., Rosenberg, M. (Eds. ), Microbial Cell Surface Hydrophobicity. American Society for Microbiology, 1990, Washington, DC, USA, pp.75-105.

[8] C. Paulo, M. Dittrich, 2D Raman spectroscopy study of dolomite and cyanobacterial extracellular polymeric substances from Khor Al-Adaid sabkha (Qatar), Journal of Raman Spectroscopy (2013) 1563–1569.

DOI: 10.1002/jrs.4368

[9] O. Braissant, G. Cailleau, C. Dupraz, E.P. Verrecchia, Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acids, Journal of Sea Research 73 (2003) 485-490.

DOI: 10.1306/111302730485

[10] M. Dittrich, S. Sibler, Calcium carbonate precipitation by cyanobacterial polysaccharides, Geological Society, London, Special Publications 336 (2010) 51-63.

DOI: 10.1144/sp336.4

[11] A. Liang, C. Paulo, Y. Zhu, M. Dittrich, CaCO3 biomineralization on cyanobacterial surfaces: Insights from experiments with three Synechococcus strains, Colloids and Surfaces B: Biointerfaces 111 (2013) 600–608.

DOI: 10.1016/j.colsurfb.2013.07.012

[12] M. Obst, J.J. Dynes, J.R. Lawrence, G.D.W. Swerhone, K. Benzerara, C. Karundakaran, K. Kaznatcheev, T. Tyliszcak, A.P. Hitchcock, Precipitation of amorphous CaCO3 (aragonite-like) by cyanobacteria: a STXM study of the influence of EPS on the nucleation process, Geochimica et Cosmochimica Acta 73 (2009).

DOI: 10.1016/j.gca.2009.04.013

[13] M. Obst, B. Wehrli, M. Dittrich, CaCO3 nucleation by cyanobacteria: laboratory evidence for a passive, surface-induced mechanism, Geobiology 7 (2009) 324–347.

DOI: 10.1111/j.1472-4669.2009.00200.x

[14] C. Vasconcelos, M. Dittrich, J.A. McKenzie, Evidence of microbiocoenosis in the formation of laminae in modern stromatolites, Facies 60 (2013) 3–13.

DOI: 10.1007/s10347-013-0371-3

[15] C. Dupraz, P.T. Visscher, Microbial lithification in marine stromatolites and hypersaline mats, Trends in Microbiology 13 (2005) 429-438.

DOI: 10.1016/j.tim.2005.07.008

[16] M.M. Tice, D.R. Lowe, Hydrogen-based carbon fixation in the earliest known photosynthetic organisms, Geology 34 (2006) 37-40.

DOI: 10.1130/g22012.1

[17] J.W. Schopf, Fossil evidence of Archean life. Philosophical Transactions of the Royal Society, B 361 (2006) 869-885.

[18] C. Dupraz, R.P. Reid, O. Braissant, A.W. Decho, R.S. Norman, P.Y. Visscher, Processes of carbonate precipitation in modern microbial mats, Earth-Science Reviews 96 (2009) 141-162.

DOI: 10.1016/j.earscirev.2008.10.005

[19] P.T. Visscher, J.F. Stolz, Microbial mats as bioreactors: populations, processes and products, Palaeogeography, Palaeoclimatology, Palaeoecology 219 (2005) 87-100.

DOI: 10.1016/j.palaeo.2004.10.016

[20] T. Bosak, S.E. Greene, D.K. Newman, A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites, Geobiology 5 (2007) 119-126.

DOI: 10.1111/j.1472-4669.2007.00104.x

[21] J.M. Olson, R.E. Blankenship, Thinking about the evolution of photosynthesis, Photosynthesis Research 80 (2004) 373-386.

DOI: 10.1023/b:pres.0000030457.06495.83

[22] J.B. Ries, Review: geological and experimental evidence for secular variation in seawater Mg/Ca (calcite-aragonite seas) and its effects on marine biological calcification, Biogeosciences 7 (2010) 2795-2849.

DOI: 10.5194/bg-7-2795-2010

[23] M.U.E. Merz, W.R. Schlue, H. Zankl, The biology of carbonate precipitation by cyanobacteria, Facies 26 (1992) 81-102.

[24] D. Papineau, J.J. Walker, S.J. Mojzsis, N.R. Pace, Composition and structure of microbial communities from stromatolites of Hamelin pool in Shark Bay, Western Australia, Applied and Environmental Microbiology 71 (2005) 4822-4832.

DOI: 10.1128/aem.71.8.4822-4832.2005

[25] G.A. Zavarzin, V.K. Orleansky, L.M. Gerasimenko., S.N. Pushko, Laboratory models of cyano-microbial mats of alkaline geochemical barrier, Microbiology 72 (2003) 93-98 (in Russian).

[26] J.B. Thompson, F.G. Ferris, Cyanobacterial precipitation of gypsum, calcite, and magnesite from natural alkaline lake water, Geology 18 (1990) 995–998.

DOI: 10.1130/0091-7613(1990)018<0995:cpogca>2.3.co;2

[27] A.M. Hartley, W.A. House, M.E. Callow, B.S.C. Leadbeate, The role of green algae in the precipitation of calcite and the coprecipitation of phosphate in freshwater, Internationale Revue der gesamten Hydrobiologie und Hydrographie 80 (1995).

DOI: 10.1002/iroh.19950800302

[28] S. Douglas, T.J. Beveridge, Mineral formation by bacteria in natural microbial communities, FEMS Microbiology Ecology 26 (1998) 79-88.

DOI: 10.1111/j.1574-6941.1998.tb00494.x

[29] M. Obst, M. Dittrich, Calcium adsorption and changes of the surface microtopography of cyanobacteria studied by AFM, CFM, and TEM with respect to biogenic calcite nucleation, Geochemistry Geophysics Geosystems 7 (2006) 15.

DOI: 10.1029/2005gc001172

[30] M. Dittrich, S. Sibler, Calcium carbonate precipitation by cyanobacterial polysaccharides, Geological Society, London, Special Publications 336 (2010) 51-63.

DOI: 10.1144/sp336.4

[31] S.A. Kranz, D. Wolf-Gladrow, G. Nehrke, G. Langer, B. Rost, Calcium carbonate precipitation induced by the growth of the marine cyanobacterium Trichodesmium. Limnology and Oceanography 55 (2010) 2563-2569.

DOI: 10.4319/lo.2010.55.6.2563

[32] R.E. Martinez, E. Gardés, O.S. Pokrovsky, J. Schott, E.H. Oelkers, Do photosynthetic bacteria have a protective mechanism against carbonate precipitation at their surfaces? Geochimica et Cosmochimica Acta 74 (2010) 1329-1337.

DOI: 10.1016/j.gca.2009.11.025

[33] V.M. Vasconcelos, K. Sivonen, W.L.R. Evans, W.W. Carmichael, M. Namikoshi, Isolation and characterization of microcystins (heptapeptide hepatotoxins) from Portuguese strains of Microcystis aeruginosa Kutz Emend Elekin. Archiv für Hydrobiologie 134 (1995).

DOI: 10.1127/archiv-hydrobiol/134/1995/295

[34] R. Warthmann, Y. Van Lith, C. Vasconcelos, J.A. McKenzie, A.M. Karpoff, Bacterially induced dolomite precipitation in anoxic culture experiments, Geology 28 (2000) 1091-1094.

DOI: 10.1130/0091-7613(2000)028<1091:bidpia>2.3.co;2

[35] Y. Van Lith, C. Vasconcelos, R. Warthmann, J.A. McKenzie, Microbial fossilization in carbonate sediments; a result of the bacterial surface involvement in carbonate precipitation, Sedimentology 50 (2003) 237–245.

DOI: 10.1046/j.1365-3091.2003.00550.x

[36] T.R.R. Bontognali, C. Vasconcelos, R.J. Warthmann, C. Dupraz, S.M. Bernasconi, J.A. McKenzie, Microbes produce nanobacteria-like structures, avoiding cell entombment, Geology 36 (2008) 663-666.

DOI: 10.1130/g24755a.1

[37] P.A. Kenward, R.H. Goldstein, L.A. Gonzalez, J.A. Roberts, Precipitation of low-temperature dolomite from an anaerobic microbial consortium: the role of methanogenic Archaea, Geobiology 7 (2009) 556–565.

DOI: 10.1111/j.1472-4669.2009.00210.x

[38] F. G. Ferris, V. Phoenix, Y. Fujita, R.W. Smith, Kinetics of calcite precipitation induced by ureolytic bacteria at 10 to 20°C in artificial groundwater, Geochimica et Cosmochimica Acta 68 (2004) 1701-1710.

DOI: 10.1016/s0016-7037(03)00503-9

[39] A.C. Mitchell, F.G. Ferris, The coprecipitation of Sr into calcite precipitates induced by bacterial ureolysis in artificial groundwater: Temperature and kinetic dependence, Geochimica et Cosmochimica Acta 69 (2005) 4199-4210.

DOI: 10.1016/j.gca.2005.03.014

[40] M. Sánchez-Román, C.S. Romanek, D.C. Fernández-Remolar, A. Sánchez-Navas, J.A. McKenzie, R.A. Pibernat, C. Vasconcelos, Aerobic biomineralization of Mg-rich carbonates: Implications for natural environments, Chemical Geology 281 (2011) 143-150.

DOI: 10.1016/j.chemgeo.2010.11.020

[41] B. Lian, Q. Hu, J. Chen, J. Ji, H.H. Teng, Carbonate biomineralization induced by soil bacterium Bacillus megaterium, Geochimica et Cosmochimica Acta 70 (2006) 5522-5535.

DOI: 10.1016/j.gca.2006.08.044

[42] G. Aloisi, A. Gloter, M. Kruger, K. Wallmann, F. Guyot, P. Zuddas, Nucleation of calcium carbonate on bacterial nanoglobules, Geology 34 (2006) 1017-1020.

DOI: 10.1130/g22986a.1

[43] Imhoff J.F., Taxonomy and physiology of phototrophic purple bacteria and green sulfur bacteria. In: Blankenship, R., Madigan, M. T, Bauer, C.E. (Eds), Anoxygenic Photosynthetic Bacteria, Springer, 2004, The Netherlands, pp.1-15.

DOI: 10.1007/0-306-47954-0_1

[44] V.M. Gorlenko, E.I. Kompantseva, S.A. Korotkov, N.N. Pouchkova, A.S. Savvichev, Development conditions and species of phototrophic bacteria, inhabiting salty shallow reservoirs in Crimea, Izvestiya AN SSSR Seriya Biologia 3 (1984).

[45] E.I. Kompantseva, A.V. Komova, N.A. Kostrikina, Rhodovulum steppense sp. nov., an obligately haloalkaliphilic purple nonsulfur bacterium widespread in saline soda lakes of Central Asia, International Journal of Systematic and Evolutionary Microbiology 60 (2010).

DOI: 10.1099/ijs.0.014639-0

[46] E.I. Kompantseva, A.V. Komova, V.I. Krauzova, T.V. Kolganova, A.N. Panteleeva, Purple nonsulfur bacteria in weakly and moderately mineralized soda lakes of the Southern Transbaikal region and Northeastern Mongolia, Microbiology 78 (2009) 246-253.

DOI: 10.1134/s0026261709020179

[47] E.I. Kompantseva, Rhodobacter euryhalinus sp. nov., a new halophilic purple bacterial species, Mikrobiologiya 54 (1985) 974-982.

[48] C. Jansson, T. Northen, Calcifying cyanobacteria – the potential of biomineralization for carbon capture and storage, Current Opinion in Biotechnology 21 (2010) 365-371.

DOI: 10.1016/j.copbio.2010.03.017

[49] O.A. Koksharova, Application of molecular genetic and microbiological techniques in ecology and biotechnology of cyanobacteria, Microbiology 79 (2010) 734-747.

DOI: 10.1134/s0026261710060020

[50] A. J Smith, The Biology of Cyanobacteria, In: Carr, N. G. & Whitton, B. A. (eds), University of California Press, Berkeley (1982) 47-85.

[51] B.D. Lee, W.A. Appel, M.R. Walton, Whitings as a Potential Mechanism for Controlling Atmospheric Carbon Dioxide Concentrations, Final Project Report, INL/EXT-06-01351, Idaho National Laboratory (2006).

DOI: 10.2172/911640

[52] H. Beraldi-Campesi, S.R. S Cevallos-Ferriz, E. Chacón-Baca, Microfossil algae associated with Cretaceous stromatolites in the Tarahumara Formation, Sonora, Mexico, Cretaceous Research 25 (2004) 249-265.

DOI: 10.1016/j.cretres.2003.12.002

[53] M.T. Madigan, J.M. Martinko, J. Parker, Brock Biology of Microorganisms 9th edition. Prentice Hall. Upper Saddle River, NJ, 2000, 991 pp.

[54] S. Stocks-Fischer, J.K. Galinat, S.S. Bang, Microbiological precipitation of CaCO3, Soil Biology and Biochemistry 31 (1999) 1563-1571.

DOI: 10.1016/s0038-0717(99)00082-6