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Abstract

Micro-organisms contribute to Earth’s mineral deposits through a process known as bacteria-induced mineral precipitation (BIMP). It is a complex phenomenon that can occur as a result of a variety of physiological activities that influence the supersaturation state and nucleation catalysis of mineral precipitation in the environment. There is a good understanding of BIMP induced by bacterial metabolism through the control of metal redox states and enzyme-mediated reactions such as ureolysis. However, other forms of BIMP often cannot be attributed to a single pathway but rather appear to be a passive result of bacterial activity, where minerals form as a result of metabolic by-products and surface interactions within the surrounding environment. BIMP from such processes has formed the basis of many new innovative biotechnologies, such as soil consolidation, heavy metal remediation, restoration of historic buildings and even self-healing concrete. However, these applications to date have primarily incorporated BIMP-capable bacteria sampled from the environment, while detailed investigations of the underpinning mechanisms have been lagging behind. This review covers our current mechanistic understanding of bacterial activities that indirectly influence BIMP and highlights the complexity and connectivity between the different cellular and metabolic processes involved. Ultimately, detailed insights will facilitate the rational design of application-specific BIMP technologies and deepen our understanding of how bacteria are shaping our world.

Funding
This study was supported by the:
  • Engineering and Physical Sciences Research Council (Award EP/PO2081X/1)
    • Principle Award Recipient: SusanneGebhard
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2021-04-21
2021-05-12
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References

  1. Zavarzin GA. [Microbial geochemical calcium cycle]. Mikrobiologiia 2002; 71:1–17 [CrossRef][PubMed]
    [Google Scholar]
  2. Banks ED, Taylor NM, Gulley J, Lubbers BR, Giarrizo JG et al. Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. Geomicrobiol J 2010; 27:444–454 [CrossRef]
    [Google Scholar]
  3. Kaźmierczak J, Fenchel T, Kühl M, Kempe S, Kremer B et al. Caco3 precipitation in multilayered cyanobacterial mats: clues to explain the alternation of micrite and sparite layers in calcareous stromatolites. Life 2015; 5:744–769
    [Google Scholar]
  4. Riding R. Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 2000; 47:179–214 [CrossRef]
    [Google Scholar]
  5. Adolphe JP, Loubière JF, Paradas J, Soleilhavoup F. Procédé de traitement biologique d’une surface artificielle. European Patent 1990; 8903517:
    [Google Scholar]
  6. Jonkers HM. Self Healing Concrete: A Biological Approach. In van der Zwaag S. editor Self Healing Materials: An Alternative Approach to 20 Centuries of Materials Science Dordrecht: Springer Netherlands; 2007 pp 195–204
    [Google Scholar]
  7. Sharma TK, Alazhari M, Heath A, Paine K, Cooper RM. Alkaliphilic Bacillus species show potential application in concrete crack repair by virtue of rapid spore production and germination then extracellular calcite formation. J Appl Microbiol 2017; 122:1233–1244 [CrossRef][PubMed]
    [Google Scholar]
  8. Tan L, Reeksting B, Ferrandiz-Mas V, Heath A, Gebhard S et al. Effect of carbonation on bacteria-based self-healing of cementitious composites. Constr Build Mater 2020; 257:119501 [CrossRef]
    [Google Scholar]
  9. Anbu P, Kang C-H, Shin Y-J, So J-S. Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus 2016; 5:250 [CrossRef][PubMed]
    [Google Scholar]
  10. Arias D, Cisternas L, Rivas M. Biomineralization mediated by ureolytic bacteria applied to water treatment: a review. Crystals 2017; 7:345
    [Google Scholar]
  11. Dhami NK, Reddy MS, Mukherjee A. Bacillus megaterium mediated mineralization of calcium carbonate as biogenic surface treatment of green building materials. World J Microbiol Biotechnol 2013; 29:2397–2406 [CrossRef][PubMed]
    [Google Scholar]
  12. De Muynck W, De Belie N, Verstraete W. Microbial carbonate precipitation in construction materials: a review. Ecological Engineering 2010; 36:118–136
    [Google Scholar]
  13. Phillips AJ, Gerlach R, Lauchnor E, Mitchell AC, Cunningham AB et al. Engineered applications of ureolytic biomineralization: a review. Biofouling 2013; 29:715–733
    [Google Scholar]
  14. Zhu T, Dittrich M. Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. Front Bioeng Biotechnol 2016; 4:1–21 [CrossRef]
    [Google Scholar]
  15. Bazylinski DA, Frankel RB, Konhauser KO. Modes of biomineralization of magnetite by microbes. Geomicrobiol J 2007; 24:465–475 [CrossRef]
    [Google Scholar]
  16. Konhauser K, Riding R. Bacterial Biomineralization. Fundamentals of Geobiology Chichester, UK: John Wiley & Sons, Ltd; 2012 pp 105–130
    [Google Scholar]
  17. Marvasi M, Visscher PT, Perito B, Mastromei G, Casillas-Martínez L. Physiological requirements for carbonate precipitation during biofilm development of Bacillus subtilis etfA mutant. FEMS Microbiol Ecol 2010; 71:341–350 [CrossRef][PubMed]
    [Google Scholar]
  18. Baumgartner J, Morin G, Menguy N, Perez Gonzalez T, Widdrat M et al. Magnetotactic bacteria form magnetite from a phosphate-rich ferric hydroxide via nanometric ferric (oxyhydr)oxide intermediates. Proc Natl Acad Sci U S A 2013; 110:14883–14888 [CrossRef][PubMed]
    [Google Scholar]
  19. Yamagishi A, Tanaka M, Lenders JJM, Thiesbrummel J, Sommerdijk NAJM et al. Control of magnetite nanocrystal morphology in magnetotactic bacteria by regulation of mms7 gene expression. Sci Rep 2016; 6:1–11 [CrossRef]
    [Google Scholar]
  20. Arias D, Cisternas LA, Rivas M. Biomineralization of calcium and magnesium crystals from seawater by halotolerant bacteria isolated from Atacama Salar (Chile) [Online]. Desalination 2017; 405:1–9
    [Google Scholar]
  21. Prozorov T. Magnetic microbes: bacterial magnetite biomineralization. Semin Cell Dev Biol 2015; 46:36–43 [CrossRef]
    [Google Scholar]
  22. Bazylinski DA, Frankel RB. Biologically controlled mineralization in prokaryotes. Reviews in Mineralogy and Geochemistry 2003; 54:217–247 [CrossRef]
    [Google Scholar]
  23. Konhauser K. Cell surface reactivity and metal sorption. Introduction to Geomicrobiology Blackwell: Oxford; 2007
    [Google Scholar]
  24. Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS et al. Processes of carbonate precipitation in modern microbial mats. Earth-Science Reviews 2009; 96:141–162 [CrossRef]
    [Google Scholar]
  25. Benning LG, Waychunas GA. Nucleation, Growth, and Aggregation of Mineral Phases: Mechanisms and Kinetic Controls. In Brantley SL, Kubicki JD, White AF. (editors) Kinetics of Water-Rock Interaction New York, NY: Springer New York; 2008 pp 259–333
    [Google Scholar]
  26. Cubillas P, Anderson MW. Synthesis Mechanism: Crystal Growth and Nucleation. In Čejka J, Corma A, Zones S. (editors) Zeolites and Catalysis: Synthesis, Reactions and Applications Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA; 2010 pp 1–55
    [Google Scholar]
  27. Fortin D, Ferris FG, Beveridge TJ. Surface-Mediated mineral development by bacteria. Reviews in Mineralogy and Geochemistry 1997; 35:161–180
    [Google Scholar]
  28. Reeder RJ, Lamble GM, Northrup PA. XAFS study of the coordination and local relaxation around Co2+, Zn2+, Pb2+, and Ba2+ trace elements in calcite. American Mineralogist 1999; 84:1049–1060 [CrossRef]
    [Google Scholar]
  29. Schultze-Lam S, Fortin D, Davis BS, Beveridge TJ. Mineralization of bacterial surfaces. Chem Geol 1996; 132:171–181 [CrossRef]
    [Google Scholar]
  30. Boquet E, Boronat A, Ramos-Cormenzana A. Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 1973; 246:527–529
    [Google Scholar]
  31. Krajewska B. Urease-aided calcium carbonate mineralization for engineering applications: a review. J Adv Res 2018; 13:59-67 [CrossRef][PubMed]
    [Google Scholar]
  32. Reeksting BJ, Hoffmann TD, Tan L, Paine K, Gebhard S. In-Depth profiling of calcite precipitation by environmental bacteria reveals fundamental mechanistic differences with relevance to application. Appl Environ Microbiol 2020; 86:e02739–19 [CrossRef]
    [Google Scholar]
  33. Seifan M, Berenjian A. Microbially induced calcium carbonate precipitation: a widespread phenomenon in the biological world. Appl Microbiol Biotechnol 2019; 103:4693–4708 [CrossRef][PubMed]
    [Google Scholar]
  34. Basnakova G, Stephens ER, Thaller MC, Rossolini GM, Macaskie LE. The use of Escherichia coli bearing a phoN gene for the removal of uranium and nickel from aqueous flows. Appl Microbiol Biotechnol 1998; 50:266–272 [CrossRef][PubMed]
    [Google Scholar]
  35. Lauchnor EG, Schultz LN, Bugni S, Mitchell AC, Cunningham AB et al. Bacterially induced calcium carbonate precipitation and strontium Coprecipitation in a porous media flow system. Environ Sci Technol 2013; 47:1557–1564 [CrossRef][PubMed]
    [Google Scholar]
  36. Podda F, Zuddas P, Minacci A, Pepi M, Baldi F. Heavy metal coprecipitation with hydrozincite [Zn5(CO3)2(OH)6] from mine waters caused by photosynthetic microorganisms. Appl Environ Microbiol 2000; 66:5092–5098
    [Google Scholar]
  37. Beveridge TJ, Fyfe WS. Metal fixation by bacterial cell walls. Can J Earth Sci 1985; 22:1893–1898 [CrossRef]
    [Google Scholar]
  38. Douglas S, Beveridge TJ. Mineral formation by bacteria in natural microbial communities. FEMS Microbiol Ecol 1998; 26:79–88 [CrossRef]
    [Google Scholar]
  39. Madigan MT, Bender KS, Buckley DH, Sattley MW, Stahl DA. Brock Biology of Microorganisms, 15th ed. New York, USA: Pearson Higher Education; 2018
    [Google Scholar]
  40. Merroun ML, Raff J, Rossberg A, Hennig C, Reich T et al. Complexation of uranium by cells and S-layer sheets of Bacillus sphaericus JG-A12. Appl Environ Microbiol 2005; 71:5532–5543 [CrossRef][PubMed]
    [Google Scholar]
  41. Schultze-Lam S, Harauz G, Beveridge TJ. Participation of a cyanobacterial S layer in fine-grain mineral formation. J Bacteriol 1992; 174:7971–7981 [CrossRef][PubMed]
    [Google Scholar]
  42. Sleytr UB, Schuster B, Egelseer E-M, Pum D. S-layers: principles and applications. FEMS Microbiol Rev 2014; 38:823–864 [CrossRef][PubMed]
    [Google Scholar]
  43. Southam G. Bacterial surface-mediated mineral formation. In Lovley DR. editor Environmental Microbe-Metal Interactions American Society of Microbiology; 2000 pp 257–276
    [Google Scholar]
  44. Merroun ML, Nedelkova M, Ojeda JJ, Reitz T, Fernández ML et al. Bio-precipitation of uranium by two bacterial isolates recovered from extreme environments as estimated by potentiometric titration, TEM and X-ray absorption spectroscopic analyses. J Hazard Mater 2011; 197:1–10 [CrossRef][PubMed]
    [Google Scholar]
  45. Warren LA, Haack EA. Biogeochemical controls on metal behaviour in freshwater environments. Earth-Science Reviews 2001; 54:261–320 [CrossRef]
    [Google Scholar]
  46. Beveridge TJ, Murray RG. Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol 1980; 141:876–887 [CrossRef][PubMed]
    [Google Scholar]
  47. Doyle RJ, Matthews TH, Streips UN. Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall. J Bacteriol 1980; 143:471–480 [CrossRef][PubMed]
    [Google Scholar]
  48. Thomas KJ, Rice CV. Revised model of calcium and magnesium binding to the bacterial cell wall. Biometals 2014; 27:1361–1370 [CrossRef][PubMed]
    [Google Scholar]
  49. Bäuerlein E. Biomineralization of unicellular organisms: an unusual membrane biochemistry for the production of inorganic nano- and microstructures. Angewandte Chemie - International Edition 2003; 42:614–641
    [Google Scholar]
  50. Roberts JA, Kenward PA, Fowle DA, Goldstein RH, González LA et al. Surface chemistry allows for abiotic precipitation of dolomite at low temperature. Proc Natl Acad Sci U S A 2013; 110:14540–14545 [CrossRef][PubMed]
    [Google Scholar]
  51. Katz AK, Glusker JP, Markham GD, Bock CW. Deprotonation of water in the presence of carboxylate and magnesium ions. J Phys Chem B 1998; 102:6342–6350 [CrossRef]
    [Google Scholar]
  52. Kluge S, Weston J. Can a hydroxide ligand trigger a change in the coordination number of magnesium ions in biological systems?. Biochemistry 2005; 44:4877–4885 [CrossRef][PubMed]
    [Google Scholar]
  53. Purcell EM. Life at low Reynolds number. Am J Phys 1977; 45:3–11 [CrossRef]
    [Google Scholar]
  54. Thompson JB, Ferris FG. Cyanobacterial precipitation of gypsum, calcite, and magnesite from natural alkaline lake water. Geology 1990; 18:995–998 [CrossRef]
    [Google Scholar]
  55. Buczynski C, Chafetz HS. Habit of bacterially induced precipitates of calcium carbonate and the influence of medium viscosity on mineralogy. Journal of Sedimentary Research 1991; 61:226–233 [CrossRef]
    [Google Scholar]
  56. Gilbert PUPA, Albrecht M, Frazer BH. The Organic-Mineral interface in Biominerals. Reviews in Mineralogy and Geochemistry 2005; 59:157–185 [CrossRef]
    [Google Scholar]
  57. Jürgensen A, Widmeyer JR, Gordon RA, Bendell-Young LI, Moore MM et al. The structure of the manganese oxide on the sheath of the bacterium Leptothrix discophora : An XAFS study. American Mineralogist 2004; 89:1110–1118 [CrossRef]
    [Google Scholar]
  58. Braissant O, Cailleau G, Dupraz C, Verrecchia EP. Bacterially induced mineralization of calcium carbonate in terrestrial environments: the role of exopolysaccharides and amino acids. Journal of Sedimentary Research 2003; 73:485–490
    [Google Scholar]
  59. Frankel RB, Bazylinski DA. Biologically induced mineralization by bacteria. Reviews in Mineralogy and Geochemistry 2003; 54:95–114 [CrossRef]
    [Google Scholar]
  60. Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM et al. Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 2007; 5:401–411
    [Google Scholar]
  61. Ercole C, Cacchio P, Botta AL, Centi V, Lepidi A. Bacterially induced mineralization of calcium carbonate: the role of exopolysaccharides and capsular polysaccharides. Microsc Microanal 2007; 13:42–50 [CrossRef][PubMed]
    [Google Scholar]
  62. Fishman MR, Giglio K, Fay D, Filiatrault MJ. Physiological and genetic characterization of calcium phosphate precipitation by Pseudomonas species. Scientific Reports 2018; 8:1–14
    [Google Scholar]
  63. Kim HJ, Shin B, Lee YS, Park W. Modulation of calcium carbonate precipitation by exopolysaccharide in Bacillus sp. JH7. Appl Microbiol Biotechnol 2017; 101:6551–6561 [CrossRef][PubMed]
    [Google Scholar]
  64. Dupraz C, Visscher PT. Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol 2005; 13:429–438 [CrossRef][PubMed]
    [Google Scholar]
  65. Kremer B, Kazmierczak J, Stal LJ. Calcium carbonate precipitation in cyanobacterial mats from sandy tidal flats of the North sea. Geobiology 2008; 6:46–56
    [Google Scholar]
  66. Wright DT, Oren A. Nonphotosynthetic bacteria and the formation of carbonates and evaporites through time. Geomicrobiol J 2005; 22:27–53 [CrossRef]
    [Google Scholar]
  67. Fernández-Remolar DC, Preston LJ, Sánchez-Román M, Izawa MRM, Huang L et al. Carbonate precipitation under bulk acidic conditions as a potential biosignature for searching life on Mars. Earth and Planetary Science Letters 2012351–352
    [Google Scholar]
  68. Tegethoff FW. Calcium Carbonate: From the Cretaceous Period into the 21st Century Basel: Springer; 2001
    [Google Scholar]
  69. Rodriguez-Navarro C, Jimenez-Lopez C, Rodriguez-Navarro A, Gonzalez-Muñoz MT, Rodriguez-Gallego M. Bacterially mediated mineralization of vaterite. Geochim Cosmochim Acta 2007; 71:1197–1213 [CrossRef]
    [Google Scholar]
  70. Beveridge TJ, Murray RG. Uptake and retention of metals by cell walls of Bacillus subtilis. J Bacteriol 1976; 127:1502–1518 [CrossRef]
    [Google Scholar]
  71. Beveridge TJ, Koval SF. Binding of metals to cell envelopes of Escherichia coli K-12. Appl Environ Microbiol 1981; 42:325–335 [CrossRef][PubMed]
    [Google Scholar]
  72. Schultze-Lam S, Beveridge TJ. Nucleation of celestite and strontianite on a cyanobacterial S-layer. Appl Environ Microbiol 1994; 60:447–453 [CrossRef][PubMed]
    [Google Scholar]
  73. Deng H, Shen XC, Wang X-M, Du C. Calcium carbonate crystallization controlled by functional groups: a mini-review. Front Mater Sci 2013; 7:62–68 [CrossRef]
    [Google Scholar]
  74. Rivadeneyra A, Gonzalez-Martinez A, Gonzalez-Lopez J, Martin-Ramos D, Martinez-Toledo M et al. Precipitation of phosphate minerals by microorganisms isolated from a fixed-biofilm reactor used for the treatment of domestic wastewater. Int J Environ Res Public Health 2014; 11:3689–3704 [CrossRef]
    [Google Scholar]
  75. Yates KK, Robbins LL. Production of carbonate sediments by a unicellular green alga. American Mineralogist 1998; 83:1503–1509 [CrossRef]
    [Google Scholar]
  76. Picard A, Gartman A, Clarke DR, Girguis PR. Sulfate-reducing bacteria influence the nucleation and growth of mackinawite and greigite. Geochimica et Cosmochimica Acta 2018; 220:367–384
    [Google Scholar]
  77. Velásquez L, Dussan J. Biosorption and bioaccumulation of heavy metals on dead and living biomass of Bacillus sphaericus . J Hazard Mater 2009; 167:713–716 [CrossRef][PubMed]
    [Google Scholar]
  78. Benzerara K, Menguy N, Guyot F, Skouri F, de Luca G et al. Biologically controlled precipitation of calcium phosphate by Ramlibacter tataouinensis. Earth Planet Sci Lett 2004; 228:439–449 [CrossRef]
    [Google Scholar]
  79. Aloisi G, Gloter A, Krüger M, Wallmann K, Guyot F et al. Nucleation of calcium carbonate on bacterial nanoglobules. Geology 2006; 34:1017 [CrossRef]
    [Google Scholar]
  80. Bontognali TRR, Vasconcelos C, Warthmann RJ, Dupraz C, Bernasconi SM et al. Microbes produce nanobacteria-like structures, avoiding cell entombment. Geology 2008; 36:663–666
    [Google Scholar]
  81. Asada R, Tazaki K. Silica biomineralization of unicellular microbes under strongly acidic conditions. The Canadian Mineralogist 2001; 39:1–16 [CrossRef]
    [Google Scholar]
  82. Urrutia Mera M, Kemper M, Doyle R, Beveridge TJ. The membrane-induced proton motive force influences the metal binding ability of Bacillus subtilis cell walls. Appl Environ Microbiol 1992; 58:3837–3844 [CrossRef][PubMed]
    [Google Scholar]
  83. Martinez RE, Gardés E, Pokrovsky OS, Schott J, Oelkers EH. Do photosynthetic bacteria have a protective mechanism against carbonate precipitation at their surfaces?. Geochimica et Cosmochimica Acta 2010; 74:1329–1337
    [Google Scholar]
  84. Martinez RE, Pokrovsky OS, Schott J, Oelkers EH. Surface charge and zeta-potential of metabolically active and dead cyanobacteria. J Colloid Interface Sci 2008; 323:317–325 [CrossRef][PubMed]
    [Google Scholar]
  85. Hammes F, Verstraete* W. Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev Environ Sci Biotechnol 2002; 1:3–7 [CrossRef]
    [Google Scholar]
  86. Silva-Castro GA, Uad I, Gonzalez-Martinez A, Rivadeneyra A, Gonzalez-Lopez J et al. Bioprecipitation of calcium carbonate crystals by bacteria isolated from saline environments grown in culture media amended with seawater and real brine. Biomed Res Int 2015; 2015:1–12 [CrossRef][PubMed]
    [Google Scholar]
  87. Dhami NK, Reddy MS, Mukherjee A. Biomineralization of calcium carbonates and their engineered applications: a review. Front Microbiol 2013; 4:1–13 [CrossRef]
    [Google Scholar]
  88. Mitchell AC, Ferris FG, Grant Ferris F. The influence of Bacillus pasteurii on the nucleation and growth of calcium carbonate. Geomicrobiol J 2006; 23:213–226 [CrossRef]
    [Google Scholar]
  89. Sánchez-Román M, Rivadeneyra MA, Vasconcelos C, McKenzie JA. Biomineralization of carbonate and phosphate by moderately halophilic bacteria. FEMS Microbiol Ecol 2007; 61:273–284 [CrossRef][PubMed]
    [Google Scholar]
  90. Silva-Castro GA, Uad I, Rivadeneyra A, Vilchez JI, Martin-Ramos D et al. Carbonate precipitation of bacterial strains isolated from sediments and seawater: formation mechanisms. Geomicrobiol J 2013; 30:840–850 [CrossRef]
    [Google Scholar]
  91. Bosak T, Newman DK. Microbial kinetic controls on calcite morphology in supersaturated solutions. J Sed Res 2005; 75:190–199 [CrossRef]
    [Google Scholar]
  92. Gat D, Tsesarsky M, Shamir D, Ronen Z. Accelerated microbial-induced CaCO3precipitation in a defined coculture of ureolytic and non-ureolytic bacteria. Biogeosciences 2014; 11:2561–2569
    [Google Scholar]
  93. Rodriguez-Navarro C, Jroundi F, Schiro M, Ruiz-Agudo E, González-Muñoz MT. Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: implications for stone conservation. Appl Environ Microbiol 2012; 78:4017–4029 [CrossRef][PubMed]
    [Google Scholar]
  94. Zeebe RE, Wolf-Gladrow D. CO2 in Seawater: Equilibrium, Kinetics, Isotopes Amsterdam; New York: Elsevier Science Publishers B.V.; 2001
    [Google Scholar]
  95. Castro-Alonso MJ, Montañez-Hernandez LE, Sanchez-Muñoz MA, Macias Franco MR, Narayanasamy R et al. Microbially induced calcium carbonate precipitation (MICP) and its potential in Bioconcrete: microbiological and molecular concepts. Frontiers in Materials 2019; 6:1–15
    [Google Scholar]
  96. Krause S, Liebetrau V, Löscher CR, Böhm F, Gorb S et al. Marine ammonification and carbonic anhydrase activity induce rapid calcium carbonate precipitation. Geochim Cosmochim Acta 2018; 243:116–132 [CrossRef]
    [Google Scholar]
  97. Ehrlich HL. Microbes as geologic agents: their role in mineral formation. Geomicrobiol J 1999; 16:135–153 [CrossRef]
    [Google Scholar]
  98. Castanier S, Le Métayer-Levrel G, Perthuisot J-P. Ca-carbonates precipitation and limestone genesis — the microbiogeologist point of view. Sedimentary Geology 1999; 126:9–23 [CrossRef]
    [Google Scholar]
  99. Visscher PT, Reid RP, Bebout BM, Hoeft SE, Macintyre IG et al. Formation of lithified micritic laminae in modern marine stromatolites (Bahamas); the role of sulfur cycling. American Mineralogist 1998; 83:1482–1493 [CrossRef]
    [Google Scholar]
  100. Martinez RJ, Beazley MJ, Taillefert M, Arakaki AK, Skolnick J et al. Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils. Environ Microbiol 2007; 9:3122–3133 [CrossRef][PubMed]
    [Google Scholar]
  101. Newsome L, Morris K, Lloyd JR. The biogeochemistry and bioremediation of uranium and other priority radionuclides. Chemical Geology 2014; 363:164–184
    [Google Scholar]
  102. Powers LG, Mills HJ, Palumbo A V, Zhang C, Delaney K et al. Introduction of a plasmid-encoded phoA gene for constitutive overproduction of alkaline phosphatase in three subsurface Pseudomonas isolates. FEMS Microbiology Ecology 2002; 41:115–123
    [Google Scholar]
  103. Macaskie LE, Bonthrone KM, Rouch DA. Phosphatase-mediated heavy metal accumulation by a Citrobacter sp. and related enterobacteria. FEMS Microbiol Lett 1994; 121:141–146 [CrossRef][PubMed]
    [Google Scholar]
  104. Dittrich M, Obst M. Are picoplankton responsible for calcite precipitation in lakes?. Ambio 2004; 33:559–564 [CrossRef][PubMed]
    [Google Scholar]
  105. Dick GJ, Torpey JW, Beveridge TJ, Tebo BM. Direct identification of a bacterial manganese(II) oxidase, the multicopper oxidase MnxG, from spores of several different marine Bacillus species. Appl Environ Microbiol 2008; 74:15271534 [CrossRef][PubMed]
    [Google Scholar]
  106. Ehrlich HL, Newman DK, Kappler A. Ehrlich’s Geomicrobiology CRC Press.; 2015
    [Google Scholar]
  107. Lovley DR. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 1991; 55:259–287 [CrossRef][PubMed]
    [Google Scholar]
  108. Reguera G, Kashefi K. The electrifying physiology of Geobacter bacteria, 30 years on. Adv Microb Physiol 2019; 74:1–96
    [Google Scholar]
  109. Anderson S, Appanna VD, Huang J, Viswanatha T. A novel role for calcite in calcium homeostasis. FEBS Lett 1992; 308:94–96 [CrossRef][PubMed]
    [Google Scholar]
  110. Yates KK, Robbins LL. Radioisotope tracer studies of inorganic carbon and Ca in microbially derived CaCO3. Geochim Cosmochim Acta 1999; 63:129–136 [CrossRef]
    [Google Scholar]
  111. Deng S, Dong H, Lv G, Jiang H, Yu B et al. Microbial dolomite precipitation using sulfate reducing and halophilic bacteria: results from Qinghai lake, Tibetan Plateau, NW China. Chemical Geology 2010; 278:151–159
    [Google Scholar]
  112. Wright DT, Wacey D. Precipitation of dolomite using sulphate-reducing bacteria from the Coorong region, South Australia: significance and implications. Sedimentology 2005; 52:987–1008 [CrossRef]
    [Google Scholar]
  113. González-Muñoz MT, De Linares C, Martínez-Ruiz F, Morcillo F, Martín-Ramos D et al. Ca-Mg kutnahorite and struvite production by Idiomarina strains at modern seawater salinities. Chemosphere 2008; 72:465–472 [CrossRef][PubMed]
    [Google Scholar]
  114. Kooli WM, Comensoli L, Maillard J, Albini M, Gelb A et al. Bacterial iron reduction and biogenic mineral formation for the stabilisation of corroded iron objects. Sci Rep 2018; 8:1–11 [CrossRef]
    [Google Scholar]
  115. González-Muñoz M, Chekroun K. Bacterially induced Mg-calcite formation: role of Mg2+ in development of crystal morphology. J Sed Res 2000; 70:559–564
    [Google Scholar]
  116. Li L, Qian C, Cheng L, Wang R. A laboratory investigation of microbe-inducing CdCO3 precipitate treatment in Cd2+ contaminated soil. J Soils Sediments 2010; 10:248–254
    [Google Scholar]
  117. Naik-Samant S, Furtado I. Formation of rhodochrosite by haloferax alexandrinus GUSF-1. J Clust Sci 2019; 30:1435–1441
    [Google Scholar]
  118. Kang C-H, Oh SJ, Shin Y, Han S-H, Nam I-H et al. Bioremediation of lead by ureolytic bacteria isolated from soil at abandoned metal mines in South Korea. Ecol Eng 2015; 74:402–407 [CrossRef]
    [Google Scholar]
  119. Ngwenya BT, Magennis M, Podda F, Gromov A. Self-preservation strategies during bacterial biomineralization with reference to hydrozincite and implications for fossilization of bacteria. J R Soc Interface 2014; 11:20140845 [CrossRef][PubMed]
    [Google Scholar]
  120. Power IM, Wilson SA, Thom JM, Dipple GM, Southam G. Biologically induced mineralization of dypingite by cyanobacteria from an alkaline wetland near Atlin, British Columbia, Canada. Geochemical Transactions 2007; 8:1–16
    [Google Scholar]
  121. Sanchez-Moral S, Luque L, Cañaveras JC, Laiz L, Jurado V et al. Bioinduced barium precipitation in St. Callixtus and Domitilla catacombs. Annals of Microbiology 2004; 54:1–12
    [Google Scholar]
  122. Rivadeneyra MA, Ramos-Cormenzana A, Garcia-Cervigon A. Formation of bobierrite (magnesium phosphate) crystal aggregates by Acinetobacter sp. Mineral J 1987; 13:443–447 [CrossRef]
    [Google Scholar]
  123. Macaskie L, Empson R, Cheetham A, Grey C, Skarnulis A. Uranium bioaccumulation by a Citrobacter sp. as a result of enzymically mediated growth of polycrystalline HUO2PO4. Science 1992; 257:782–784
    [Google Scholar]
  124. Crosby CH, Bailey JV. The role of microbes in the formation of modern and ancient phosphatic mineral deposits. Front Microbiol 2012; 3:1–7 [CrossRef]
    [Google Scholar]
  125. Chen Z, Pan X, Chen H, Guan X, Lin Z. Biomineralization of Pb(II) into Pb-hydroxyapatite induced by Bacillus cereus 12-2 isolated from Lead-Zinc mine tailings. J Hazard Mater 2016; 301:531–537 [CrossRef][PubMed]
    [Google Scholar]
  126. Konhauser KO. Bacterial iron biomineralisation in nature. FEMS Microbiol Rev 1997; 20:315–326 [CrossRef]
    [Google Scholar]
  127. Konhauser KO, Fyfe WS, Schultze-Lam S, Ferris FG, Beveridge TJ. Iron phosphate precipitation by epilithic microbial biofilms in Arctic Canada. Can J Earth Sci 1994; 31:1320–1324 [CrossRef]
    [Google Scholar]
  128. Biswas M, Majumdar S, Chowdhury T, Chattopadhyay B, Mandal S et al. Bioremediase a unique protein from a novel bacterium BKH1, ushering a new hope in concrete technology. Enzyme Microb Technol 2010; 46:581–587 [CrossRef]
    [Google Scholar]
  129. Yee N, Phoenix VR, Konhauser KO, Benning LG, Ferris FG. The effect of cyanobacteria on silica precipitation at neutral pH: implications for bacterial silicification in geothermal hot springs. Chem Geol 2003; 199:83–90 [CrossRef]
    [Google Scholar]
  130. Ta K, Peng X, Chen S, Xu H, Li J et al. Hydrothermal nontronite formation associated with microbes from low-temperature diffuse hydrothermal vents at the South Mid-Atlantic Ridge. J Geophys Res 2017; 122:2375–2392 [CrossRef]
    [Google Scholar]
  131. Lefèvre CT, Menguy N, Abreu F, Lins U, Pósfai M et al. A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science 2011; 334:1720–1723
    [Google Scholar]
  132. Thiel J, Byrne JM, Kappler A, Schink B, Pester M. Pyrite formation from FeS and H 2 S is mediated through microbial redox activity. Proceedings of the National Academy of Sciences of the United States of America ; 2019
  133. Gramp JP, Sasaki K, Bigham JM, Karnachuk OV, Tuovinen OH. Formation of covellite (cus) under biological sulfate-reducing conditions. Geomicrobiol J 2006; 23:613619 [CrossRef]
    [Google Scholar]
  134. Karnachuk OV, Sasaki K, Gerasimchuk AL, Sukhanova O, Ivasenko DA et al. Precipitation of Cu-sulfides by copper-tolerant Desulfovibrio isolates. Geomicrobiol J 2008; 25:219227 [CrossRef]
    [Google Scholar]
  135. Labrenz M, Druschel GK, Thomsen-Ebert T, Gilbert B, Welch SA et al. Formation of sphalerite (ZnS) deposits in natural biofilms of sulfate-reducing bacteria. Science 2000
    [Google Scholar]
  136. Wolicka D, Borkowski A. Influence of electron donors and copper concentration on geochemical and mineralogical processes under conditions of biological sulphate reduction. Acta Geologica Polonica 2014; 64:138–146 [CrossRef]
    [Google Scholar]
  137. Keren R, Mayzel B, Lavy A, Polishchuk I, Levy D et al. Sponge-associated bacteria mineralize arsenic and barium on intracellular vesicles. Nat Commun 2017; 8:1–12 [CrossRef]
    [Google Scholar]
  138. Polgári M, Gyollai I, Fintor K, Horváth H, Pál-Molnár E et al. Microbially mediated ore-forming processes and cell mineralization. Front Microbiol 2019; 10:
    [Google Scholar]
  139. Greene AC, Madgwick JC. Microbial formation of manganese oxides. Appl Environ Microbiol 1991; 57:1114–1120 [CrossRef][PubMed]
    [Google Scholar]
  140. Villalobos M, Toner B, Bargar J, Sposito G. Characterization of the manganese oxide produced by Pseudomonas putida strain MnB1. Geochim Cosmochim Acta 2003; 67:2649–2662 [CrossRef]
    [Google Scholar]
  141. Webb SM, Tebo BM, Bargar JR. Structural characterization of biogenic Mn oxides produced in seawater by the marine Bacillus sp. strain SG-1. American Mineralogist 2005; 90:1342–1357 [CrossRef]
    [Google Scholar]
  142. Mandernack KW, Post J, Tebo BM. Manganese mineral formation by bacterial spores of the marine Bacillus, strain SG-1: Evidence for the direct oxidation of Mn(II) to Mn(IV). Geochimica et Cosmochimica Acta 1995
    [Google Scholar]
  143. Lovley DR, Phillips EJ. Reduction of uranium by Desulfovibrio desulfuricans . Appl Environ Microbiol 1992; 58:850–856 [CrossRef][PubMed]
    [Google Scholar]
  144. Roh Y, Liu SV, Li G, Huang H, Phelps TJ et al. Isolation and characterization of metal-reducing Thermoanaerobacter strains from deep subsurface environments of the Piceance Basin, Colorado. Appl Environ Microbiol 2002; 68:6013–6020 [CrossRef][PubMed]
    [Google Scholar]
  145. Suzuki Y, Kelly SD, Kemner KM, Banfield JF. Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Appl Environ Microbiol 2003; 69:1337–1346 [CrossRef][PubMed]
    [Google Scholar]
  146. Achal V, Pan X, Fu Q, Zhang D. Biomineralization based remediation of As(III) contaminated soil by Sporosarcina ginsengisoli. J Hazard Mater 2012; 201-202:178–184 [CrossRef][PubMed]
    [Google Scholar]
  147. Seifan M, Berenjian A. Application of microbially induced calcium carbonate precipitation in designing bio self-healing concrete. World J Microbiol Biotechnol 2018; 34:168 [CrossRef][PubMed]
    [Google Scholar]
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