Advertisement

Calcite formation induced by Ensifer adhaerens, Microbacterium testaceum, Paeniglutamicibacter kerguelensis, Pseudomonas protegens and Rheinheimera texasensis

  • Kouta Hatayama
  • Katsumi Saito
Original Paper
  • 62 Downloads

Abstract

A wide range of bacterial species are able to induce calcium carbonate precipitation. Using our own laboratory-preserved strains, we have newly discovered that Ensifer sp. MY11e, Microbacterium sp. TMd9a1, Paeniglutamicibacter sp. MSa1a, Pseudomonas sp. GTc3, and Rheinheimera sp. ATWe6 can induce the formation of calcite crystals on an agar medium. Type strains of their closely related species (Ensifer adhaerens, Microbacterium testaceum, Paeniglutamicibacter kerguelensis, Pseudomonas protegens, and Rheinheimera texasensis) could also induce calcite formation. Although the initial pH value of the agar medium was 6.1, the pH of the agar media containing calcite, induced by cultivation of the 10 bacterial strains, increased to 8.0–8.4. The ammonification (oxidative deamination) of amino acids may been responsible for this increase in pH. The crystals formed both on and around the bacterial colonies. Furthermore, when these strains (excepting two Microbacterium strains) were cultivated on a cellulose acetate membrane filter (0.20 μm pore size) resting on the surface of the agar medium (i.e., in the membrane filter culture method), the crystals formed on the agar medium separate from the bacterial cells. These results indicate that the bacterial cells did not necessarily become nucleation sites for these crystals. We also investigated whether the studied strains could be applied to the biocementation of sand, and found that only two Ensifer strains were able to form large sand lumps.

Keywords

Biomineralization Calcium carbonate precipitation Calcite Biocementation 

Notes

Authors’ contributions

KH conceived of the study, carried out the experiments and wrote the manuscript. KS contributed to the experiments, discussion and preparation of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10482_2018_1204_MOESM1_ESM.pdf (1.8 mb)
Supplementary material 1 (PDF 1857 kb)

References

  1. Aloisi G, Gloter A, Krüger M, Wallmann K, Guyot F, Zuddas P (2006) Nucleation of calcium carbonate on bacterial nanoglobules. Geology 34:1017–1020CrossRefGoogle Scholar
  2. Anbu P, Kang C-H, Shin Y-J, So J-S (2016) Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus 5:250CrossRefGoogle Scholar
  3. Bansal R, Dhami NK, Mukherjee A, Reddy MS (2016) Biocalcification by halophilic bacteria for remediation of concrete structures in marine environment. J Ind Microbiol Biotechnol 43:1497–1505CrossRefGoogle Scholar
  4. Bazylinski DA, Frankel RB (2003) Biologically controlled mineralization in prokaryotes. Rev Mineral Geochem 54:217–247CrossRefGoogle Scholar
  5. Boquet E, Boronat A, Ramos-Cormenzana A (1973) Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246:527–529CrossRefGoogle Scholar
  6. Bosak T, Newman DK (2005) Microbial kinetic controls on calcite morphology in supersaturated solutions. J Sediment Res 75:190–199CrossRefGoogle Scholar
  7. Casida LE (1982) Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in soil. Int J Syst Bacteriol 32:339–345CrossRefGoogle Scholar
  8. Daskalakis MI, Magoulas A, Kotoulas G, Catsikis I, Bakolas A, Karageorgis AP, Mavridou A, Doulia D, Rigas F (2013) Pseudomonas, Pantoea and Cupriavidus isolates induce calcium carbonate precipitation for biorestoration of ornamental stone. J Appl Microbiol 115:409–423CrossRefGoogle Scholar
  9. De Muynck W, De Belie N, Verstraete W (2010) Microbial carbonate precipitation in construction materials: a review. Ecol Eng 36:118–136CrossRefGoogle Scholar
  10. Dhami NK, Reddy MS, Mukherjee A (2013a) Biomineralization of calcium carbonates and their engineered applications: a review. Front Microbiol 4:314CrossRefGoogle Scholar
  11. Dhami NK, Reddy MS, Mukherjee A (2013b) Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. J Microbiol Biotechnol 23:707–714CrossRefGoogle Scholar
  12. Ganendra G, De Muynck W, Ho A, Arvaniti EC, Hosseinkhani B, Ramos JA, Rahier H, Boon N (2014) Formate oxidation-driven calcium carbonate precipitation by Methylocystis parvus OBBP. Appl Environ Microbiol 80:4659–4667CrossRefGoogle Scholar
  13. Ghashghaei S, Emtiazi G (2013) Production of calcite nanocrystal by a urease-positive strain of Enterobacter ludwigii and study of its structure by SEM. Curr Microbiol 67:406–413CrossRefGoogle Scholar
  14. González-Muñoz MT, Rodriguez-Navarro C, Martínez-Ruiz F, Arias JM, Merroun ML, Rodriguez-Gallego M (2010) Bacterial biomineralization: new insights from Myxococcus-induced mineral precipitation. Geol Soc Spec Publ 336:31–50CrossRefGoogle Scholar
  15. Gupta P, Reddy GS, Delille D, Shivaji S (2004) Arthrobacter gangotriensis sp. nov. and Arthrobacter kerguelensis sp. nov. from Antarctica. Int J Syst Evol Microbiol 54:2375–2378CrossRefGoogle Scholar
  16. Hatayama K (2014) Comamonas humi sp. nov., isolated from soil. Int J Syst Evol Microbiol 64:3976–3982CrossRefGoogle Scholar
  17. Hatayama K, Kuno T (2015a) Spirosoma fluviale sp. nov., isolated from river water. Int J Syst Evol Microbiol 65:3447–3450CrossRefGoogle Scholar
  18. Hatayama K, Kuno T (2015b) Croceifilum oryzae gen. nov., sp. nov., isolated from rice paddy soil. Int J Syst Evol Microbiol 65:4061–4065CrossRefGoogle Scholar
  19. Hatayama K, Kawai S, Shoun H, Ueda Y, Nakamura A (2005) Pseudomonas azotifigens sp. nov., a novel nitrogen-fixing bacterium isolated from a compost pile. Int J Syst Evol Microbiol 55:1539–1544CrossRefGoogle Scholar
  20. Hatayama K, Esaki K, Ide T (2013) Cellulomonas soli sp. nov. and Cellulomonas oligotrophica sp. nov., isolated from soil. Int J Syst Evol Microbiol 63:60–65CrossRefGoogle Scholar
  21. Hatayama K, Ushida A, Kuno T (2016) Flavobacterium aquicola sp. nov., isolated from river water. Int J Syst Evol Microbiol 66:2789–2796CrossRefGoogle Scholar
  22. Heidari Nonakaran S, Pazhouhandeh M, Keyvani A, Abdollahipour FZ, Shirzad A (2015) Isolation and identification of Pseudomonas azotoformans for induced calcite precipitation. World J Microbiol Biotechnol 31:1993–2001CrossRefGoogle Scholar
  23. Jansson C, Northen T (2010) Calcifying cyanobacteria—the potential of biomineralization for carbon capture and storage. Curr Opin Biotechnol 21:365–371CrossRefGoogle Scholar
  24. Kim JH, Lee J, Park J, Gho YS (2015) Gram-negative and gram-positive bacterial extracellular vesicles. Semin Cell Dev Biol 40:97–104CrossRefGoogle Scholar
  25. Komagata K, Iizuka H (1964) New species of Brevibacterium isolated from rice (Studies on the microorganisms of cereal grains. Part VII). Nippon Nogeikagaku Kaishi 38:496–502 (in Japanese) CrossRefGoogle Scholar
  26. Lowenstam HA (1981) Minerals formed by organisms. Science 211:1126–1131CrossRefGoogle Scholar
  27. Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press, OxfordGoogle Scholar
  28. Maciejewska M, Adam D, Naômé A, Martinet L, Tenconi E, Całusińska M, Delfosse P, Hanikenne M, Baurain D, Compère P, Carnol M, Barton HA, Rigali S (2017) Assessment of the potential role of Streptomyces in cave moonmilk formation. Front Microbiol 8:1181CrossRefGoogle Scholar
  29. Martin D, Dodds K, Butler IB, Ngwenya BT (2013) Carbonate precipitation under pressure for bioengineering in the anaerobic subsurface via denitrification. Environ Sci Technol 47:8692–8699PubMedGoogle Scholar
  30. Merchant MM, Welsh AK, McLean RJ (2007) Rheinheimera texasensis sp. nov., a halointolerant freshwater oligotroph. Int J Syst Evol Microbiol 57:2376–2380CrossRefGoogle Scholar
  31. Park S-J, Park Y-M, Chun W-Y, Kim W-J, Ghim S-Y (2010) Calcite-forming bacteria for compressive strength improvement in mortar. J Microbiol Biotechnol 20:782–788PubMedGoogle Scholar
  32. Ramette A, Frapolli M, Fischer-Le Saux M, Gruffaz C, Meyer J-M, Défago G, Sutra L, Moënne-Loccoz Y (2011) Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Syst Appl Microbiol 34:180–188CrossRefGoogle Scholar
  33. Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49:1–7PubMedPubMedCentralGoogle Scholar
  34. Wei S, Cui H, Jiang Z, Liu H, He H, Fang N (2015) Biomineralization processes of calcite induced by bacteria isolated from marine sediments. Braz J Microbiol 46:455–464CrossRefGoogle Scholar
  35. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617CrossRefGoogle Scholar
  36. Zhu T, Dittrich M (2016) Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. Front Bioeng Biotechnol 4:4CrossRefGoogle Scholar
  37. Zhu Y, Ma N, Jin W, Wu S, Sun C (2017) Genomic and transcriptomic insights into calcium carbonate biomineralization by marine actinobacterium Brevibacterium linens BS258. Front Microbiol 8:602PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Sagami Chemical Research InstituteAyaseJapan
  2. 2.Department of Applied ChemistryTokai UniversityHiratsukaJapan

Personalised recommendations