Effect of the tryptone concentration on the calcium carbonate biomineralization mediated by Bacillus cereus
Efecto de la concentración de triptona en la biomineralización de carbonato de calcio mediada por Bacillus cereus
DOI:
https://doi.org/10.15446/dyna.v85n205.60637Palabras clave:
Bacillus cereus, biomineralization, calcium carbonate, tryptone, calcite, vaterite (en)Bacillus cereus, biomineralización, carbonato de calcio, triptona, calcita, vaterita (es)
Descargas
Recibido: 21 de octubre de 2016; Revisión recibida: 13 de noviembre de 2017; Aceptado: 25 de enero de 2018
Abstract
Five tryptone concentrations (0.2%, 0.4%, 0.6%, 0.8% and 1.0%) were evaluated on calcium carbonate biomineralization processes, using 0.5% of calcium acetate. A culture of Bacillus cereus, isolated from the gardens of The Universidad Pontificia Bolivariana (Medellin, Antioquia, Colombia) was used in all the assays. The experiments were monitored by pH measurements and mineralogical analyses of X-ray diffraction (XRD), Fourier transform infrared spectroscopy (FTIR) and Scanning electronic microscopy (SEM). Vaterite was the predominant polymorph in the precipitates after 6 days of the process. However, a considerable proportion of calcite appeared (above 30%) when the tryptone concentration was 0.4% or below. Additionally, the other experiments had a similar precipitate formation (between 3.2-3.6 g/L) except the assay using 0.2% of tryptone, which presented a low calcium carbonate production (1.79 g/L). A tryptone concentration below 0.4% would limit the bacterial metabolism and CO2 formation, necessary for calcium carbonate production.
Keywords:
Bacillus cereus, biomineralization, calcium carbonate, tryptone, calcite, vaterite.Resumen
Se evaluaron cinco concentraciones de triptona (0.2%, 0.4%, 0.6%, 0.8% y 1.0%) en procesos de biomineralización de carbonato de calcio, utilizando acetato de calcio al 0.5%. Todos los ensayos se hicieron con una cepa de Bacillus cereus, aislada de los jardines de la Universidad Pontificia Bolivariana (Medellín, Antioquia, Colombia). Los experimentos fueron monitoreados con mediciones de pH y análisis mineralógicos de difracción de rayos X (XRD), espectroscopía de infrarrojo con transformada de Fourier (FTIR) y microscopía electrónica de barrido (SEM). La vaterita fue el polimorfo predominante en los precipitados después de 6 días de proceso. Sin embargo, una proporción considerable de calcita (por encima de 30%) apareció cuando la concentración de triptona fue de 0.4% y menor. Adicionalmente, los experimentos tuvieron una formación de precipitados similar (entre 3.2 y 3.6 g/L), menos el ensayo con 0.2% de triptona, que presentó una baja producción de carbonato de calcio (1.79 g/L), indicando que una concentración de triptona menor a 0.4% limitaría el metabolismo bacteriano y la formación de CO2, necesaria para la producción de carbonato de calcio.
Palabras clave:
Bacillus cereus, biomineralización, carbonato de calcio, triptona, calcita, vaterita.1. Introduction
The biomineralization of calcium carbonate is a process associated with eukaryotic and prokaryotic physiologies. In the bacterial world, many microorganisms are capable of precipitating calcium carbonate crystals in the form of calcite or vaterite [1]. The bacteria of the genus Bacillus spp. (mainly Bacillus subtilis, Bacillus pasteurii, Bacillus amyloliquefaciens, Bacillus cereus) are ones of the most widely known. This microorganism require CO2 dissolved in the medium (in the form of HCO3 2- and CO3 2-) and a defined source of calcium (generally as a salt) to carry out the biocrystallization of calcium carbonate [2]. It is believed that the microorganisms produce an induced biomineralization (activated), where the bacteria regulate the calcium entry and exit through of a protein-non protein channel. The Ca2+ ions expelled by the bacterium in presence of CO3 2- facilitate the formation of calcium carbonate [3,4].
The ability to precipitate calcium carbonate crystals is continuously studied, because of its multiple applications in the industries of construction, bioremediation, medicine, cosmetics and others [5,6]. It is noteworthy that the formation of calcium carbonate is a complex process that can be manipulated in several ways. The control of the morphology and the size of the crystals are very important, considering its final application. The kind of the obtained mineral depends on several conditions of the medium, including temperature, saturation, pH as well as the presence of additives and impurities [7].
In general, the culture media employed in the induced biomineralization processes of calcium carbonate require a calcium salt (usually calcium acetate) and a nutritious broth, composed of various components (glucose, yeast extract, tryptone, etc.) [8-10]. In preliminary trials for this work, it was found that a strain of Bacillus cereus was capable of producing calcium carbonate from a medium that only contained 1.0% of tryptone and 0.5% of calcium acetate (data not shown).
This work evaluated the effects of reducing the tryptone concentration on the carbonate bioproduction to determine a minimum concentration of the compound that can allow an adequate carbonate precipitate index, considering a scalable process at a commercial level with a lower reactive consumption. All the obtained precipitates were mineralogically analyzed to observe if there were morphologic and or polymorphic variations.
2. Experimental procedure
2.1. Microorganism
A pure culture of Bacillus cereus was selected for the experiments. It was isolated from soil material from the gardens of the Universidad Pontificia Bolivariana (Medellin, Colombia). The strain was adapted prior to the calcium carbonate biomineralization process. The adaptation consisted in several subcultures in a modified M3 medium (0.5% calcium acetate and 1.0% tryptone) up to observe no variations on pH and the quantity of precipitate generated between the replicas.
The inocula were prepared in a 250 mL erlenmeyer, using different concentrations of tryptone for each bacterial assay (from 0.2% to 1.0%). The working volume was 100 mL and the culture composition had a ratio of 1 mL of inoculum per 9 mL of M3 modified medium (evaluating the respective tryptone concentration) [9]. The strains were incubated for 6 days in an orbital agitator at a temperature of 30°C ± 1°C and an agitation velocity of 180 rpm ± 2 rpm.
2.2. Biomineralization of calcium carbonate
Each assay was prepared in a 250 mL erlenmeyer (working volume of 100 mL), using a ratio of 1 mL bacteria inoculum per 9 mL or modified M3 modified medium. The variable evaluated was the tryptone concentration (%w): 0.2, 0.4, 0.6, 0.8 and 1.0.
All assays were incubated for 6 days under temperature and agitation conditions like the used in the preparation of the inocula. The experiments also had their respective replica and abiotic control (without presence of microorganisms). Additionally, the pH was periodically monitored for each sample, using an HACH HQ 30d pH meter.
At the end of each assay, 80 mL were extracted from each erlenmeyer and centrifuged at 3500 rpm for 10 minutes. After this time, the supernatant was discarded and the precipitate was washed 4 times with distilled water and other 4 times with ethylic alcohol (90 %v), agitating in a vortex for 1 minute and then centrifuging at 3500 rpm for 10 minutes. Afterwards, the samples were dried at room temperature. The final product was used to determine the amount of formed precipitate per liter of medium, dividing the obtained weight over the sample volume.
2.3. Mineralogical analyses
The mineralogical composition of the samples was established with X-ray diffraction (XRD), Fourier transform infrared analysis (FTIR) and scanning electronic microscopy (SEM). For all the analyses, the original sample was used, without particle size transformations.
The XRD analyses were made in a Rigaku Miniflex II diffractometer, using the step by step method, with 5° start angle, 70° stop angle, 0.05° step angle, and counting time of 50 s. The minerals present in the precipitate were quantified using a Rietveld refinement in the X’Pert HighScore Plus© software with the PDF-4-2012 database and the American Mineralogist Crystal Structure Database [11].
The FTIR analyses were carried out in a Thermo Scientific Nicolet spectrometer, using the ATR method with the pure sample, using an interval of 400-4000 cm-1, 32 scans and a spectral resolution of 4 cm-1.
For the SEM analyses, the sample was coated with a fine silver layer. The “sputtering” (cathodic pulverization) coating technique was performed with a DENTON VACCUM DESK IV. The analysis was carried in a JEOL JSM-6490LV sweep electron microscope. Additionally, an Oxford Instruments INCA PentaFETx3 X-ray-EDX analyzer was employed to carry out the microchemical sample analyses.
3. Results and discussion
3.1. Biomineralization of calcium carbonate
Fig. 1 illustrates the pH behavior, where all the assays had a continuous increase of the value. Probably, the bacterial growth could have affected this parameter, because Bacillus cereus is heterotrophic and it is able to carry out the aerobic ammonification process of amino acids in presence of dissolved oxygen, organic matter and calcium [6].
Figure 1: pH vs. time during the calcium bioprecipitation process at different tryptone concentrations.
According to Periasiami et al. (2016), the microorganisms might be able to produce carbonate compounds (CO3 2−) during its cellular growth and metabolism activation. This compounds might have reacted with Ca2+ ions (from calcium acetate), affecting the acid-base environment in the culture medium [12].
Although the assays using a tryptone concentration ≥ 0.4% tended to stabilize at day 6 of the process, the assay using 0.2% of tryptone decreased its raising from the second day. The final pH for all assays were around 9 and the highest values were achieved by the assays using tryptone concentrations of 0.6% (9.19) and 0.8% (9.18), followed by the 0.4% (9.08), 1.0% (8.98) and 0.2% (8.92) tests.
The differences among pH tendency can be explained by the availability of energy source. A high tryptone concentration might imply a higher access to proteins necessaries to bacterial multiplication, giving as result a higher carbonate compounds and therefore alkalization of the medium [13,14].
Fig. 2 presents the quantity of precipitate obtained in each assay. The assays with tryptone concentration higher than 0.4% obtained values above 3.2 grams of precipitate per liter of solution. The highest precipitate quantity was obtained in the assays with 0.8% (3.56 g/L) and 1.0% (3.58 g/L). In contrast, the assay using 0.2% tryptone obtained the lowest precipitation, 44.5% lower than the experiment with the subsequent precipitate concentration (3.23 g/L).
Figure 2: Obtained precipitate during the calcium bioprecipitation process at different tryptone concentrations.
The precipitation of calcium carbonate observed in the assays using the highest concentrations tryptone (Fig. 2) might be related with the propagation and metabolism of the microorganism which promote the mineral synthesis, either segregating metabolites which accelerating CO2 hydration, regulating CO2 y HCO3 - concentrations and modifying pH of the medium, as shown in eq. (1) and eq. (2) [15,16]. For the last reason, calcium carbonate biomineralization is product of the quantity of CO3 2− and Ca2+ ions in the medium.
3.2. Mineralogical analyses
Fig. 3 shows the diffractograms of the precipitates for all the assays using different tryptone concentrations. The presence of calcium carbonate was identified in two crystalline phases: vaterite and calcite, where vaterite was the predominant polymorph. Notwithstanding, the assays using 0.2% and 0.4% of tryptone presented a greater intensity in the calcite peaks in comparison to the other experiments. On the other hand, none of the assays presented formations of other minerals.
Figure 3: Diffractograms of the precipitates for each trial at different tryptone (T) concentrations. Va: vaterite, Ca: calcite
From Rietveld refinement of the XRD patterns (Fig. 1), Table 1 presents the semi-quantitative ratios of the crystalline phases of both vaterite and calcite for all the precipitates. The weighted residual profile of the refinements (Rwp) was below 10% which did not vary more than 20% with respect to the residual expected (Rexp). These parameters determined that the refinement models were good to accept the values obtained [17-19]. The assays with the three highest tryptone concentrations had a greater vaterite formation (above 97%), while the percentage of calcite was increased considerably when concentrations below 0.4% tryptone were used.
Source: The authors.Table 1: Percentage of calcite and vaterite in crystalline phase of the obtained precipitates in the tests at different tryptone concentrations.
Wei et al. (2015), explain that the polymorphism of carbonate biomineralization to calcite, vaterite or aragonite depends of the environmental conditions and the culture medium. Additionally, different types of bacteria can precipitate calcium carbonate with diverse crystalline structure (spherical or polyhedral) or even amorphous forms [20].
Bacillus cereus is an ureolytic bacterium which promotes the production of calcium carbonate when the culture medium is enriched with a protein source, as tryptone. For this purpose, the microorganism activates the biochemical metabolism of the enzyme urease [1]. Although vaterite is the less stable among the three polymorphs of anhydrous calcium carbonate at environmental conditions and it tends to transform into calcite, several research have found stability of bio-vaterite by biomolecules from the cellular wall of the bacteria, where compounds with phosphorus ions, carboxylic groups or polysaccharides play an important key role to coordinate calcium and carbonate orientation [1].
Based on the results of this work, the reduction of the main nutrient source below 0.4% probably reduce the synthesis of the biomolecules that maintain the stability of vaterite, thus it might have allowed a transformation of a part of calcium carbonate into calcite.
Fig. 4 shows the FTIR spectra for all the precipitates and Table 2 presents the bands identification with their respective assignations. The presence of calcite and vaterite was validated for all assays. The band at 713 cm-1, corresponding to calcite, indicated the greatest presence of this mineral in the assays with 0.2% and 0.4% of tryptone. The bands at 1280 cm-1 and 1707-1725 cm-1 indicated that the precipitates had traces of organic matter after the washing phase, probably originating from one of the compounds of the cultivation medium. The band at 1648-1653 cm-1 signaled the presence of natural humidity of the sample and the band at 3282-3300 cm-1 indicates interactions of O-H, possibly corresponding to the to the residual alcohol from the washing phase of the precipitates [21,22].
Figure 4: FTIR spectra of the precipitates for each test at different tryptone (T) concentrations.
Table 2: Bands of the FTIR spectra for the obtained precipitates at different tryptone concentrations.
Fig. 5 illustrates SEM images. All the precipitates presented a cylindrical, hollow structure formation pattern with an external diameter of approximately 1 µm and variable lengths between 5 µm and 15 µm, possibly originated from the biomineralization of calcium carbonate nanoparticles over the microorganisms. Probably, the bacteria had a surface with charged nucleation sites where the mineral could initialize its generation [23]. The samples of the assays with the highest tryptone concentrations (Fig. 5d) also presented other typical structures, including spherical particles which correspond to the formation of vaterite [29]. Other formations founded were ramified carbonate less than 1 micron (Fig. 5h), product of particles that did not probably tend to form the shells of microorganisms. The accumulation of some particles (Fig. 5i) could be attributed to the washing phase of the precipitates.
Figure 5: SEM images of the precipitates of the tests at varying tryptone concentrations. Formation of bacillary structures from the biomineralized microorganisms of the tests 0.2% T (a), 0.4% T (b), 0.6% T (c) and 1.0% T (e). Accumulation of vaterite spheres in the 0.8% T (d) test. Magnification of the precipitates of test 0.4% T which indicates that the cylindrical structures are hollow (f). Coating of the shells with stem shaped mineral growths (g and h) and accumulation of agglomerate particles (i).
From the SEM and EDS analyses, microchemical analyses were carried out to some of the structures found in the precipitates (Fig. 5). Fig. 6 and Table 3 illustrates the particles that covered the biomineralized shells of the microorganisms (assay 0.4% T), where a low calcium concentration and a high carbon concentration was identified. Comparing with the ideal atomic relations of calcium carbonate (1 Ca:1 C:3 O), it indicates that the particles or their surroundings presented components of organic matter possibly from precipitated organic compounds, product of the reaction mechanisms of the microorganisms or traces of the bacteria that were within the structures.
Figure 6: EDS of the particles that coated the shells of the biomineralized microorganisms (test 0.4% T)
Source: The authors.Table 3: Microchemical analysis of particles that coated the shells of the biomineralized microorganisms (Fig. 6).
Fig. 7 and Table 4 shows the microchemical analysis of the surface of a shell (assay 0.4% T). The highest calcium peak indicates a higher purity in the structure. Notwithstanding, the high carbon content indicates the presence of residual organic matter in the surroundings.
Figure 7: EDS of the shell of the biomineralized microorganisms (test 0.4% T).
Source: The authors.Table 4: Microchemical analysis of the biomineralized microorganisms (Fig. 7).
Fig. 8 and Table 5 shows the microchemical analysis of an accumulation of particles (assay 0.4% T). As was observed in Fig. 6 and Fig. 7, the high amount of carbon indicates the presence of residual organic matter in the surroundings.
The mineral formation over the bacterial surface could have presented in two stages:
Figure 8: EDS of shell accumulations of the biomineralized microorganisms (test 0.4% T).
Source: The authors.Table 5: Microchemical analysis of shell accumulations of the biomineralized microorganisms (Fig. 8).
The possible reaction in the nucleation sites mediated by Ca2+ ions by the mechanism showed in the eq. (3) to eq. (5) [33]. In first place, the metallic ions from the medium might have stoichiometrically interacted with the charges groups of the bacterial surface structures, allowing the mineral deposition and generating bacillary walls, as observed in Fig. 5 to Fig. 7 [34].
After precipitation, the second stage implies the increasing of the calcium carbonate concentration and saturation of the cell surface, generating an agglomeration and precipitation outside the cell, as shown Fig. 8. This precipitation is not controlled by the microorganism, but by the physic-chemical environment of the surface around each bacterium.
On the other hand, the traces of phosphorous identified in the microchemical analyses (Table 3 to Table 5) can have their origin in some of the components present in the Tryptone of the cultivation medium.
4. Conclusions
The microorganisms used in the project had a greater tendency to produce calcium carbonate nanoparticles as vaterite. The ratio of vaterite-calcite and its degree of purity can be affected by the tryptone concentration. However, a tryptone concentration below 0.4% would limit the metabolism of the bacteria and therefore the CO2 formation, which could cause a deficit in the production of the precipitate. Notwithstanding, a 0.4% concentration produced a good precipitate rate, which is comparable to the results obtained at higher concentrations.
The processes carried out allowed the formation of shell shaped structures, which are composed of calcium carbonate nanoparticles (vaterite-calcite) with a bacillary morphology and hollow core, which could be considered as “microbricks”. Because the shells do not collapse after the washing phases of the precipitate, these could have potential applications in the manufacture of osseous structures for the microencapsulation of medications due to their hollow and almost uniform distribution.
Acknowledges
To Biofenix S.A.S. and the Universidad Pontificia Bolivariana, where the investigation was carried out and RutaN (Medellin) who finances the project.
References
Referencias
Daskalakis, M.I., Rigas, F., Bakolas, A., Magoulas, A., Kotoulas, G., Katsikis, I., Karageorgis, A.P. and Mavridou, A., Vaterite bio-precipitation induced by Bacillus pumilus isolated from a solutional cave in Paiania, Athens, Greece, International Biodeterioration and Biodegradation, 99, pp. 73-84, 2015. DOI: 10.1016/J.Ibiod.2014.12.005
Stocks-Fischer, S., Galinat, J.K. and Bang, S.S., Microbiological precipitation of CaCO3. Soil Biology and Biochemistry, 31(11), pp. 1563-1571, 1999. DOI: 10.1016/S0038-0717(99)00082-6
Cacchio, P., Ercole, C., Cappuccio, G. and Lepidi, A., Calcium carbonate precipitation by bacterial strains isolated from a limestone cave and from a loamy soil. Geomicrobiology Journal, 20(2), pp. 85-98, 2003. DOI: 10.1080/01490450303883
De Muynck, W., De Belie, N. and Verstraete, W., Microbial carbonate precipitation in construction materials: a review. Ecological
Engineering, 36, pp. 118-136, 2010. DOI: 10.1016/J.Ecoleng.2009.02.006
Tiano, P., Biagiotti, L. and Mastromei, G., Bacterial bio-mediated calcite precipitation for monumental stones conservation: methods of evaluation. Journal of Microbiological Methods, 36, pp. 139-145, 1999. DOI: 10.1016/S0167-7012(99)00019-6
Castanier, S., Le Metayer-Levrel, G., Orial, G., Loubiere, J.F. and Perthuisot, J.P., Bacterial carbonatogenesis and applications to preservation and restoration of historic property, en Ciferri, O. Of Microbes and Art: The role of microbial communities in the degradation and protection of cultural heritage [online], Springer Sicence+Business Media, 2000, pp. 203-218. [consulted, October 20th of 2016]. Available at: https://goo.gl/ffsuIw
Wada, N., Yamashita, K. and Umegaki, T., Effects of carboxylic acids on calcite formation in the presence of Mg2+ ions. Journal of Colloid and Interface Science, 212, pp. 357-364, 1999. DOI: 10.1006/Jcis.1998.6067
Boquet, E., Boronat, A. and Ramos-Cormenzana, A., Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature, 246, pp. 527-529, 1973. DOI: 10.1038/246527a0
Rodriguez-Navarro, C., Rodriguez-Gallego, M., Chekroun, K.B. and Gonzalez-Muñoz, M.T., Conservation of ornamental stone by Myxococcus xanthus - induced carbonate biomineralization. Applied and Environmental Microbiology, 69(4), pp. 2182-2193, 2003. DOI: 10.1128/Aem.69.4.2182
Jimenez-Lopez, C., Jroundi, F., Pascolini, C., Rodriguez-Navarro, C., Piñar-Larrubia, G., Rodriguez-Gallego, M. and González-Muñoz, M.T., Consolidation of quarry calcarenite by calcium carbonate precipitation induced by bacteria activated among the microbiota inhabiting the stone. International Biodeterioration and Biodegradation, 62(4), pp. 352-363, 2008. DOI: 10.1016/J.Ibiod.2008.03.002
Downs, R.T. and Hall-Wallace, M., The American mineralogist crystal structure database. American Mineralogist [online], 88(1), 2003. [date of reference October 20th of 2016]. Available at: https://goo.gl/LwfD48
Anbu, P., Kang, C.-H., Shin, Y.-J. and So, J.-S., Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus, 5(250), pp. 1-26 DOI: 10.1186/S40064-016-1869-2
Baskar, S., Baskar, R., Mauclaire, L. and Mckenzie, J.A., Microbially induced calcite precipitation in culture experiments: possible origin for stalactites in Sahastradhara caves, Dehradun, India. Current Science [online], 90(1), 2006. [date of reference October 20th of 2016]. Available at: https://goo.gl/j3axfc
Rusznyák, A., Akob, D.M., Nietzsche, S., Eusterhues, K., Totsche, K.U., Neu, T.R., Torsten, F., Popp, J., Keiner, R., Geletneky, J., Katzschmann, L., Schulze, E.D. and Küsel, K., Calcite biomineralization by bacterial isolates from the recently discovered Pristine Karstic Herrenberg cave. Applied and Environmental Microbiology, 78(4), pp. 1157-1167, 2012. DOI:10.1128/Aem.06568-11
Chahal, N.K., Rajor, A. and Siddique, R. Calcium carbonate precipitation by different bacterial strains. African Journal of Biotechnology, 10(42), pp. 8359-8372, 2011. DOI: 10.5897/Ajb11.345
Weiner, S. and Dove, P.M., An overview of biomineralization processes and the problem of the vital effect. Reviews in Mineralogy and Geochemistry, 54(1), pp. 1-29, 2003. DOI: 10.2113/0540001
Mccusker, L.B., Von Dreele, R.B., Cox, D.E., Loue, D. and Scardi, P., Rietveld refinement guidelines. Journal of Applied Crystallography, 32, pp. 36-50, 1999. DOI: 10.1107/S0021889898009856
Simanjuntak, W. and Sembiring, S., The use of the Rietveld method to study the phase composition of cordierite (Mg2Al4Si5O18) ceramics prepared from rice husk silica. Makara, Sains [online], 15, 2011. [date of reference October 20th of 2016]. Available at: https://goo.gl/8RrF3w
Kniess C.T., Cardoso-de Lima, J. and Prates, P.B., The quantification of crystalline phases in materials: applications of Rietveld method, en Shatokha, V. Sintering - Methods and Products [en línea], Intech, 2012, pp. 293-316. [consulta,
de octubre de 2016]. Available at: http://goo.gl/NWoIs4
Wei, S., Cui, H., Jiang, Z., Liu, H., He, H. and Fang, N., Biomineralization processes of calcite induced by bacteria isolated from marine sediments. Brazilian Journal of Microbiology, 46(2), pp. 455-464, 2015. DOI: 10.1590/S1517-838246220140533
Wang, F., Xu, Z., Zhang, Y., Li, J., Nian, S. and Zhou, N., Green synthesis and bioactivity of vaterite-doped beta-dicalcium silicate bone cement. Ceramics International, 42(1), pp. 1856-1861, 2016. DOI: 10.1016/J.Ceramint.2015.09.150
Silverstein, R.M., Webster, F.X., Kiemle, D.J. and Bryce, D.L., Spectrometric identification of organic compounds [online], 8th Edition, Wiley Online Library, 2014 [consulted: October 20th of 2016]. Available at: https://goo.gl/gt91UY
Zhou, G.-T., Guan, Y.-B., Yao, Q.-Z. and Fu, S.-Q., Biomimetic mineralization of prismatic calcite mesocrystals: relevance to biomineralization. Chemical Geology, 279, pp. 63-72, 2010. DOI: 10.1016/J.Chemgeo.2010.08.020
Montoya, C., Márquez, M.A., López, J. y Cuervo, C., Caracterización de cristales de calcita bioprecipitada por un aislamiento nativo de Bacillus subtilis. Revista Colombiana de Biotecnología [en línea], 7(2), 2005. [Consultado: Octubre 20 de 2016]. Disponible en: https://goo.gl/GV5C0I
Patil, V.J., Patil, U.D., Bhoge, Y.E. and Kulkarni, R.D., Facile synthesis of calcium carbonate nanoparticles using solution spray reactor system. International Journal of Applied Engineering Research [online], 9(10), 2014. [date of reference October 20th of 2016]. Available at: Http://Www.Ripublication.Com/Ijaer.Htm
Wang, Y.-Y., Yao, Q.-Z., Zhou, G.-T. and Fu, S.-Q., Formation of elongated calcite mesocrystals and implication for biomineralization. Chemical Geology, 360-361, pp. 126-133, 2013. DOI: 10.1016/J.Chemgeo.2013.10.013
Singh, M., Kumar, V.S., Waghmare, S.A. and Sabale, P.D., Aragonite-vaterite-calcite: polymorphs of CaCO3 in 7th century CE lime plasters of Alampur group of temples, India. Construction and Building Materials, 112, pp. 386-397, 2016. DOI: 10.1016/J.Conbuildmat.2016.02.191
Sevcík, R., Pérez-Estébanez, M., Viani, A., Sasek, P. and Mácová, P., Characterization of vaterite synthesized at various temperatures and stirring velocities without use of additives. Powder Technology, 284, pp. 265-271, 2015. DOI: 10.1016/J.Powtec.2015.06.064
Liu, J., Liu, Y., Kong, Y., Yao, J. and Cai, Y., Formation of vaterite regulated by silk sericin and its transformation towards hydroxyapatite microsphere. Materials Letters, 110, pp. 221-224, 2013. DOI: 10.1016/J.Matlet.2013.08.021
Trushina, D.B., Bukreeva, T.V., Kovalchuk, M.V. and Antipina, M.N., CaCO3 vaterite microparticles for biomedical and personal care applications. Materials Science and Engineering C, 45, pp. 644-658, 2015. DOI: 10.1016/J.Msec.2014.04.050
Saikia, J. and Das, G., Framboidal vaterite for selective adsorption of anionic dyes. Journal of Environmental Chemical Engineering, 2(2), pp. 1165-1173, 2014. DOI: 10.1016/J.JECE.2014.04.016
dePaula, S.M., Huila, M.F.G., Araki, K. and Toma, H.E., Confocal raman and electronic microscopy studies on the topotactic conversion of calcium carbonate from Pomacea lineate shells into hydroxyapatite bioceramic materials in phosphate media. Micron, 41(8), pp. 983-989, 2010. DOI: 10.1016/J.Micron.2010.06.014
Li, W., Liu, L.-P., Zhou, P.-P., Cao, L., Yu, L.-J. and Jiang, S.-Y., Calcite precipitation induced by bacteria and bacterially produced carbonic anhydrase. Current Science [online], 100(4), 2011. [date of reference October 20th of 2016]. Available at: https://goo.gl/qp8RrA
Douglas, S. and Beveridge, T.J., Mineral formation by bacteria in natural microbial communities. FEMS Microbiology Ecology [online], 26, pp. 79-88, 1998. DOI: 10.1016/S0168-6496(98)00027-0
Cómo citar
IEEE
ACM
ACS
APA
ABNT
Chicago
Harvard
MLA
Turabian
Vancouver
Descargar cita
CrossRef Cited-by
1. Preksha Fadia, Simona Tyagi, Stuti Bhagat, Abhishek Nair, Pooja Panchal, Harsh Dave, Sadev Dang, Sanjay Singh. (2021). Calcium carbonate nano- and microparticles: synthesis methods and biological applications. 3 Biotech, 11(11) https://doi.org/10.1007/s13205-021-02995-2.
2. Marwa Eltarahony, Sahar Zaki, Desouky Abd-El-Haleem. (2020). Aerobic and anaerobic removal of lead and mercury via calcium carbonate precipitation mediated by statistically optimized nitrate reductases. Scientific Reports, 10(1) https://doi.org/10.1038/s41598-020-60951-1.
3. Naira A. Awadeen, Marwa Eltarahony, Sahar Zaki, Amany Yousef, Samy El-Assar, Hadeel El-Shall. (2024). Fungal carbonatogenesis process mediates zinc and chromium removal via statistically optimized carbonic anhydrase enzyme. Microbial Cell Factories, 23(1) https://doi.org/10.1186/s12934-024-02499-7.
4. Marwa Eltarahony, Ayman Kamal, Sahar Zaki, Desouky Abd‐El‐Haleem. (2021). Heavy metals bioremediation and water softening using ureolytic strains Metschnikowia pulcherrima and Raoultella planticola. Journal of Chemical Technology & Biotechnology, 96(11), p.3152. https://doi.org/10.1002/jctb.6868.
5. Marwa Eltarahony, Sahar Zaki, Ayman Kamal, Desouky Abd-El-Haleem. (2021). Calcite and Vaterite Biosynthesis by Nitrate Dissimilating Bacteria in Carbonatogenesis Process under Aerobic and Anaerobic Conditions. Geomicrobiology Journal, 38(9), p.791. https://doi.org/10.1080/01490451.2021.1951398.
Dimensions
PlumX
Visitas a la página del resumen del artículo
Descargas
Licencia
Derechos de autor 2018 DYNA
![Creative Commons License](http://i.creativecommons.org/l/by-nc-nd/4.0/88x31.png)
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial-SinDerivadas 4.0.
El autor o autores de un artículo aceptado para publicación en cualquiera de las revistas editadas por la facultad de Minas cederán la totalidad de los derechos patrimoniales a la Universidad Nacional de Colombia de manera gratuita, dentro de los cuáles se incluyen: el derecho a editar, publicar, reproducir y distribuir tanto en medios impresos como digitales, además de incluir en artículo en índices internacionales y/o bases de datos, de igual manera, se faculta a la editorial para utilizar las imágenes, tablas y/o cualquier material gráfico presentado en el artículo para el diseño de carátulas o posters de la misma revista.