Skip to main content
Log in

Magnesium-Calcite Crystal Formation Mediated by the Thermophilic Bacterium Geobacillus thermoglucosidasius Requires Calcium and Endospores

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Fresh Geobacillus thermoglucosidasius cells grown on soybean-casein digest nutrient agar were inoculated as a parent colony 1 cm in diameter on the surface of an agar gel containing acetate and calcium ions (calcite-promoting hydrogel) and incubated at 60 °C for 4 days, after which magnesium-calcite single crystals of 50–130 µm in size formed within the parent colony. Addition of EDTA, polyacrylic acid or N,N-dicyclohexylcarbodiimide to the calcite-forming hydrogel inhibited the parent colony from forming magnesium-calcite crystals. Inoculation of G. thermoglucosidasius on calcite-forming hydrogel containing 5 µM cadmium and 20 µM zinc resulted in a decrease in the sporulation rate from 55 to 7–8 %. Magnesium-calcite synthesis decreased relative to the sporulation rate. G. thermoglucosidasius exhibited higher adsorption/absorbance of calcium than other Geobacillus sp. that do not mediate calcite formation and higher levels of magnesium accumulation. Calcium ions contained in the calcite-promoting hydrogel and magnesium ions concentrated in G. thermoglucosidasius cells serve as the elements for magnesium-calcite synthesis. The observed decreases in sporulation rate and magnesium-calcite formation support the hypothesis that endospores act as nuclei for the synthesis of magnesium-calcite single crystals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Amor M, Busigny V, Durand-Dubief M, Tharaud M, Ona-Nguema G, Gélabert A, Guyot F (2015) Chemical signature of magnetotactic bacteria. Proc Natl Acad Sci USA 112:1699–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Beck L, Jahns T (1996) Regulation of leucine transport by intracellular pH in Bacillus pasteurii. Arch Microbiol 165:265–271

    Article  CAS  PubMed  Google Scholar 

  3. Blakemore R (1975) Magnetotactic bacteria. Science 190:377–379

    Article  CAS  PubMed  Google Scholar 

  4. Boquet E, Boronat A, Ramos-Cormenzana A (1973) Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246:527–529

    Article  Google Scholar 

  5. Bornside GH, Kallio RE (1956) Urea-hydrolyzing bacilli II.: nutritional profiles. J Bacteriol 71:655–660

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Chung JK, Yoon HE, Shin HC, Choi EY, Byeon WH (2009) Induction of growth phase-specific autolysis in Bacillus subtilis 168 by growth inhibitors. J Microbiol 47:50–59

    Article  CAS  PubMed  Google Scholar 

  7. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643

    Article  CAS  PubMed  Google Scholar 

  8. Hamilton WA (2003) Microbially influenced corrosion as a model system for the study of metal–microbe interactions: a unifying electron transfer hypothesis. Biofouling 19:65–76

    Article  CAS  PubMed  Google Scholar 

  9. He L, Xue R, Song R (2009) Formation of calcium carbonate films on chitosan substrates in the presence of polyacrylic acid. J Solid State Chem 182:1082–1087

    Article  CAS  Google Scholar 

  10. He S, Guo Z, Zhang Y, Zhang S, Wang J, Gu N (2007) Biosynthesis of gold nanoparticles using the bacteria Rhodopseudomonas capsulata. Mater Lett 61:3984–3987

    Article  CAS  Google Scholar 

  11. Hogarth C, Ellar DJ (1978) Calcium accumulation during sporulation of Bacillus megaterium KM. Biochem J 176:197–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hogarth C, Ellar DJ (1979) Energy-dependence of calcium accumulation during sporulation of Bacillus megaterium KM. Biochem J 178:627–632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kandori K, Horigami N, Yasukawa A, Ishikawa T (1997) Texture and formation mechanism of fibrous calcium hydroxyapatite particles prepared by decomposition of calcium–EDTA chelates. J Am Ceram Soc 80:1157–1164

    Article  CAS  Google Scholar 

  14. Lacriola CJ, Falk SP, Weisblum B (2013) Screen for agents that induce autolysis in Bacillus subtilis. Antimicrob Agents Chemo 57:229–234

    Article  CAS  Google Scholar 

  15. Meier KJS, Berger C, Kinkel H (2014) Increasing coccolith calcification during CO2 rise of the penultimate deglaciation (Termination II). Mar Micropaleontol 112:1–12

    Article  Google Scholar 

  16. Murai R, Yoshida N (2013) Geobacillus thermoglucosidasius endospores function as nuclei for the formation of single calcite crystals. Appl Environ Microbiol 79:3085–3090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Nakatani Y, Imagawa M, Nishihara T, Kondo M (1985) Inhibition of cortex hydrolysis during spore germination by CdCl2. Microbiol Immunol 29:119–126

    Article  CAS  PubMed  Google Scholar 

  18. Narayanan KB, Sakthivel N (2010) Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interface Sci 156:1–13

    Article  CAS  PubMed  Google Scholar 

  19. Ohse M, Takahashi K, Kadowaki Y, Kusaoke H (1995) Effects of plasmid DNA sizes and several other factors on transformation of Bacillus subtilis ISW1214 with plasmid DNA by electroporation. Biosci Biotechnol Biochem 59:1433–1437

    Article  CAS  PubMed  Google Scholar 

  20. Paasche E (2001) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40:503–529

    Article  Google Scholar 

  21. Raeymaekers L, Wuytack EY, Willems I, Michiels CW, Wuytack F (2002) Expression of a P-type Ca2+-transport ATPase in Bacillus subtilis during sporulation. Cell Calcium 32:93–103

    Article  CAS  PubMed  Google Scholar 

  22. Raut SH, Sarode DD, Lele SS (2014) Biocalcification using B. pasteurii for strengthening brick masonry civil engineering structures. World J Microbiol Biotechnol 30:191–200

    Article  CAS  PubMed  Google Scholar 

  23. Rothenstein D, Baier J, Schreiber TD, Barucha V, Bill J (2012) Influence of zinc on the calcium carbonate biomineralization of Halomonas halophila. Aqua Biosys 8:31. doi:10.1186/2046-9063-8-31

    Article  CAS  Google Scholar 

  24. Stähl S (1978) Calcium uptake and survival of Bacillus stearothermophilus. Arch Microbiol 119:17–24

    Article  PubMed  Google Scholar 

  25. Stocks-Fischer S, Galinat JK, Bang SS (1999) Microbiological precipitation of CaCO3. Soil Biol Biochem 31:1563–1571

    Article  CAS  Google Scholar 

  26. Tanaka S, Tsumura S, Yoshida N (2005) JP Patent 2005-168302

  27. Wakeman CA, Goodson JR, Zacharia VM, Winkler WC (2014) Assessment of the requirements for magnesium transporters in Bacillus subtilis. J Bacteriol 196:1206–1214

    Article  PubMed  PubMed Central  Google Scholar 

  28. Yoshida N, Higashimura E, Saeki Y (2010) Catalytic biomineralization of fluorescent calcite by the thermophilic bacterium Geobacillus thermoglucosidasius. Appl Environ Microbiol 76:7322–7327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Naoto Yoshida.

Ethics declarations

Conflict of Interest

We declare that we have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murai, R., Yoshida, N. Magnesium-Calcite Crystal Formation Mediated by the Thermophilic Bacterium Geobacillus thermoglucosidasius Requires Calcium and Endospores. Curr Microbiol 73, 696–703 (2016). https://doi.org/10.1007/s00284-016-1115-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-016-1115-8

Keywords

Navigation