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Carbonate Mineral Formation under the Influence of Limestone-Colonizing Actinobacteria: Morphology and Polymorphism.

Cao C, Jiang J, Sun H, Huang Y, Tao F, Lian B - Front Microbiol (2016)

Bottom Line: Mineralogical analyses showed that hexagonal prism calcite was only observed in the sub-surfaces of the mycelium pellets, which is a novel morphology mediated by microbes.Our analyses suggested that the effects of mycelium pellets as a molecular template almost gained an advantage over SMP both in crystal nucleation and growth, having nothing to do with biological activity.It is thereby convinced that lithophilous actinobacteria, S. luteogriseus DHS C014, owing to its advantageous genetic metabolism and filamentous structure, showed good biomineralization abilities, maybe it would have geoactive potential for biogenic carbonate in local microenvironments.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of SciencesGuiyang, China; Institute of Geochemistry, University of Chinese Academy of SciencesBeijing, China; The Key Laboratory of Biotechnology for Medicinal Plant of Jiangsu Province, School of Life Science, Jiangsu Normal UniversityXuzhou, China.

ABSTRACT
Microorganisms and their biomineralization processes are widespread in almost every environment on earth. In this work, Streptomyces luteogriseus DHS C014, a dominant lithophilous actinobacteria isolated from microbial mats on limestone rocks, was used to investigate its potential biomineralization to allow a better understanding of bacterial contributions to carbonate mineralization in nature. The ammonium carbonate free-drift method was used with mycelium pellets, culture supernatant, and spent culture of the strain. Mineralogical analyses showed that hexagonal prism calcite was only observed in the sub-surfaces of the mycelium pellets, which is a novel morphology mediated by microbes. Hemispheroidal vaterite appeared in the presence of spent culture, mainly because of the effects of soluble microbial products (SMP) during mineralization. When using the culture supernatant, doughnut-like vaterite was favored by actinobacterial mycelia, which has not yet been captured in previous studies. Our analyses suggested that the effects of mycelium pellets as a molecular template almost gained an advantage over SMP both in crystal nucleation and growth, having nothing to do with biological activity. It is thereby convinced that lithophilous actinobacteria, S. luteogriseus DHS C014, owing to its advantageous genetic metabolism and filamentous structure, showed good biomineralization abilities, maybe it would have geoactive potential for biogenic carbonate in local microenvironments.

No MeSH data available.


Related in: MedlinePlus

Morphologies of biominerals in MP treatments. (A,B) Optical micrographs of mycelia pellets before/after mineralization, respectively; (C) showing crystals with homogeneous morphology in full view; (D) showing the details of most crystals with hexagonal prism morphology and EDS spectrum obtained from the asterisked site on the (018) face (the Au peak was the result of ion sputtering used before SEM examination); (E,F) showing calcite twins and polycrystals; (G,H) showing a three-dimensional diagram simulating the hexagonal prism calcite with front and top views, respectively.
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Figure 7: Morphologies of biominerals in MP treatments. (A,B) Optical micrographs of mycelia pellets before/after mineralization, respectively; (C) showing crystals with homogeneous morphology in full view; (D) showing the details of most crystals with hexagonal prism morphology and EDS spectrum obtained from the asterisked site on the (018) face (the Au peak was the result of ion sputtering used before SEM examination); (E,F) showing calcite twins and polycrystals; (G,H) showing a three-dimensional diagram simulating the hexagonal prism calcite with front and top views, respectively.

Mentions: In MP treatments, calcite was prone to nucleate in the sub-surfaces of mycelium pellets. At the end of mineralization, these mycelium pellets (Figure 7A) observed using optical microscopy (Leica DM500B) were covered with lots of rod-shaped crystals (Figure 7B). These near-developed calcite crystals showed a hexagonal prism shape as seen upon further observation by SEM: these were significantly different from rhombohedral crystals in FM treatments. It is a novel morphology of calcite mediated by microbes, somewhat similar to the sodium salt of poly L-isocyanoalanyl-D-alanine as a crystallization template for CaCO3 (Donners et al., 2002). Most of crystals were elongated along the crystallographic c-axis with three end faces (018) expressed on each side of the crystal (Figures 7C,D). The well-defined (018) faces mostly showed sound edges, but the (100) faces and their edges were not completely developed (Figure 7D). Ca, C, and O were identified as the major elements in the hexagonal prism crystals (Figure 7D) by EDS, which was the same as that of rhombohedral calcite in FM. Sometimes, a few crystals could develop into contact twins (Figure 7E) and polycrystals (Figure 7F), presumably due to induction and steric hindrance of complex template structures. The hexagonal prism morphology of calcite was simulated using 3D Studio Max software (Autodesk 2014), giving a front view (Figure 7G), and top view (Figure 7H). The same crystals were also found in trial treatments for biomineralization in the presence of mycelium pellets which were treated by autoclaving at 121°C for 30 min. This demonstrated that the effect of the molecular template associated with the microbial cell-walls played a conspicuous role in crystal nucleation and growth, having nothing to do with biological activity. In previous studies, different microbial cells could induce rhombohedral calcite (Lian et al., 2006), vaterite covering cells (Rodriguez-Navarro et al., 2007), spherical vaterite (Tourney and Ngwenya, 2009), peanut-like vaterite (Chen et al., 2008), respectively (Table 1).


Carbonate Mineral Formation under the Influence of Limestone-Colonizing Actinobacteria: Morphology and Polymorphism.

Cao C, Jiang J, Sun H, Huang Y, Tao F, Lian B - Front Microbiol (2016)

Morphologies of biominerals in MP treatments. (A,B) Optical micrographs of mycelia pellets before/after mineralization, respectively; (C) showing crystals with homogeneous morphology in full view; (D) showing the details of most crystals with hexagonal prism morphology and EDS spectrum obtained from the asterisked site on the (018) face (the Au peak was the result of ion sputtering used before SEM examination); (E,F) showing calcite twins and polycrystals; (G,H) showing a three-dimensional diagram simulating the hexagonal prism calcite with front and top views, respectively.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834437&req=5

Figure 7: Morphologies of biominerals in MP treatments. (A,B) Optical micrographs of mycelia pellets before/after mineralization, respectively; (C) showing crystals with homogeneous morphology in full view; (D) showing the details of most crystals with hexagonal prism morphology and EDS spectrum obtained from the asterisked site on the (018) face (the Au peak was the result of ion sputtering used before SEM examination); (E,F) showing calcite twins and polycrystals; (G,H) showing a three-dimensional diagram simulating the hexagonal prism calcite with front and top views, respectively.
Mentions: In MP treatments, calcite was prone to nucleate in the sub-surfaces of mycelium pellets. At the end of mineralization, these mycelium pellets (Figure 7A) observed using optical microscopy (Leica DM500B) were covered with lots of rod-shaped crystals (Figure 7B). These near-developed calcite crystals showed a hexagonal prism shape as seen upon further observation by SEM: these were significantly different from rhombohedral crystals in FM treatments. It is a novel morphology of calcite mediated by microbes, somewhat similar to the sodium salt of poly L-isocyanoalanyl-D-alanine as a crystallization template for CaCO3 (Donners et al., 2002). Most of crystals were elongated along the crystallographic c-axis with three end faces (018) expressed on each side of the crystal (Figures 7C,D). The well-defined (018) faces mostly showed sound edges, but the (100) faces and their edges were not completely developed (Figure 7D). Ca, C, and O were identified as the major elements in the hexagonal prism crystals (Figure 7D) by EDS, which was the same as that of rhombohedral calcite in FM. Sometimes, a few crystals could develop into contact twins (Figure 7E) and polycrystals (Figure 7F), presumably due to induction and steric hindrance of complex template structures. The hexagonal prism morphology of calcite was simulated using 3D Studio Max software (Autodesk 2014), giving a front view (Figure 7G), and top view (Figure 7H). The same crystals were also found in trial treatments for biomineralization in the presence of mycelium pellets which were treated by autoclaving at 121°C for 30 min. This demonstrated that the effect of the molecular template associated with the microbial cell-walls played a conspicuous role in crystal nucleation and growth, having nothing to do with biological activity. In previous studies, different microbial cells could induce rhombohedral calcite (Lian et al., 2006), vaterite covering cells (Rodriguez-Navarro et al., 2007), spherical vaterite (Tourney and Ngwenya, 2009), peanut-like vaterite (Chen et al., 2008), respectively (Table 1).

Bottom Line: Mineralogical analyses showed that hexagonal prism calcite was only observed in the sub-surfaces of the mycelium pellets, which is a novel morphology mediated by microbes.Our analyses suggested that the effects of mycelium pellets as a molecular template almost gained an advantage over SMP both in crystal nucleation and growth, having nothing to do with biological activity.It is thereby convinced that lithophilous actinobacteria, S. luteogriseus DHS C014, owing to its advantageous genetic metabolism and filamentous structure, showed good biomineralization abilities, maybe it would have geoactive potential for biogenic carbonate in local microenvironments.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of SciencesGuiyang, China; Institute of Geochemistry, University of Chinese Academy of SciencesBeijing, China; The Key Laboratory of Biotechnology for Medicinal Plant of Jiangsu Province, School of Life Science, Jiangsu Normal UniversityXuzhou, China.

ABSTRACT
Microorganisms and their biomineralization processes are widespread in almost every environment on earth. In this work, Streptomyces luteogriseus DHS C014, a dominant lithophilous actinobacteria isolated from microbial mats on limestone rocks, was used to investigate its potential biomineralization to allow a better understanding of bacterial contributions to carbonate mineralization in nature. The ammonium carbonate free-drift method was used with mycelium pellets, culture supernatant, and spent culture of the strain. Mineralogical analyses showed that hexagonal prism calcite was only observed in the sub-surfaces of the mycelium pellets, which is a novel morphology mediated by microbes. Hemispheroidal vaterite appeared in the presence of spent culture, mainly because of the effects of soluble microbial products (SMP) during mineralization. When using the culture supernatant, doughnut-like vaterite was favored by actinobacterial mycelia, which has not yet been captured in previous studies. Our analyses suggested that the effects of mycelium pellets as a molecular template almost gained an advantage over SMP both in crystal nucleation and growth, having nothing to do with biological activity. It is thereby convinced that lithophilous actinobacteria, S. luteogriseus DHS C014, owing to its advantageous genetic metabolism and filamentous structure, showed good biomineralization abilities, maybe it would have geoactive potential for biogenic carbonate in local microenvironments.

No MeSH data available.


Related in: MedlinePlus