Crystalline Nanorods as Possible Templates for the Synthesis of Amorphous Biosilica during Spicule Formation in Demospongiae

Mugnaioli, Enrico; Natálio, Filipe; Schloßmacher, Ute; Wang, Xiaohong; Müller, Wernér E.G.; Kolb, Ute

doi:10.1002/cbic.200800623

Cited by 22 publications

(24 citation statements)

References 34 publications

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“…Morphological studies were performed by Philips EM420. Linescan and spot EDX were performed in scanning transmission electron microscopy (STEM) mode by a FEI Tecnai F30 equipped with an energy-dispersive X-ray spectrometer (Mugnaioli et al, 2009). …”

Section: Transmission Electron Microscopy and Energy-dispersive X-raymentioning

confidence: 99%

Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata

Gong

Wiens

Schröder

et al. 2010

Journal of Experimental Biology

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SUMMARYLoricate choanoflagellates (unicellular, eukaryotic flagellates; phylum Choanozoa) synthesize a basket-like siliceous lorica reinforced by costal strips (diameter of approximately 100nm and length of 3m). In the present study, the composition of these siliceous costal strips is described, using Stephanoeca diplocostata as a model. Analyses by energy-dispersive X-ray spectroscopy (EDX), coupled with transmission electron microscopy (TEM), indicate that the costal strips comprise inorganic and organic components. The organic, proteinaceous scaffold contained one major polypeptide of mass 14kDa that reacted with wheat germ agglutinin. Polyclonal antibodies were raised that allowed mapping of the proteinaceous scaffold, the (glyco)proteins, within the costal strips. Subsequent in vitro studies revealed that the organic scaffold of the costal strips stimulates polycondensation of ortho-silicic acid in a concentration-and pH-dependent way. Taken together, the data gathered indicate that the siliceous costal strips are formed around a proteinaceous scaffold that supports and maintains biosilicification. A scheme is given that outlines that the organic template guides both the axial and the lateral growth of the strips.

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Section: Transmission Electron Microscopy and Energy-dispersive X-raymentioning

confidence: 99%

Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata

Gong

Wiens

Schröder

et al. 2010

Journal of Experimental Biology

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“…Interestingly, multimetallic silicate crystals have been identified in natural sponge biosilica (26), suggesting that recombinant silicatein activity in these in vitro mineralization vesicles exhibits this natural activity as well. Our results from genetic screening showed that this crystal-forming ability could be (re)acquired via evolutionary selection for expression in a range of in vitro environments.…”

Section: Discussionmentioning

confidence: 95%

“…During in vivo formation of spicules (sponge skeletal elements; Fig. 1A), silicatein protein filaments are initially assembled intracellularly before being exported to an extracellular vesicular compartment (26,28,31). In both the in vivo and in vitro processes, silicatein enzymatically hydrolyzes precursor molecules to initiate mineralization at the silicatein filament (or silicatein-bead) surface; mineralization is templated along the silicatein scaffold, and the mineral grows radially from the scaffold surface within a shape-constraining compartment as the templating polymer becomes axially occluded within a spicule (23,28) (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Here, we combine lessons learned from silica biomineralization in marine sponges (23)(24)(25)(26)(27)(28)(29)(30)(31)(32) with emulsion-based synthetic cell surrogates (20)(21)(22) to select variants of mineralizing enzymes evolutionarily in vitro, thus advancing capabilities for studying genetically encoded inorganic materials. The cell-free enzyme reengineering method we describe is more robust for targeting a wide range of materials than cellular systems that are susceptible to poisoning or damage by certain mineral precursors or the product minerals (24).…”

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confidence: 99%

“…1), including the use of a silicatein-based scaffold with an enzymatically active surface as a catalytic template for mineralization (20,23,25,30,32) (Fig. 1A) and the ability to control reactant species within micrometer-scale compartmentalized vesicles (26,28,31). Because the amplifiable genes, their encoded silicatein-based catalytic template, and the resulting synthesized minerals all are integrated within the same vesicle-based cell surrogate, evolutionary selection works on these elements as it does in living cells.…”

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confidence: 99%

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Evolutionary selection of enzymatically synthesized semiconductors from biomimetic mineralization vesicles

Bawazer

Izumi

Kolodin

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The way nature evolves and sculpts materials using proteins inspires new approaches to materials engineering but is still not completely understood. Here, we present a cell-free synthetic biological platform to advance studies of biologically synthesized solid-state materials. This platform is capable of simultaneously exerting many of the hierarchical levels of control found in natural biomineralization, including genetic, chemical, spatial, structural, and morphological control, while supporting the evolutionary selection of new mineralizing proteins and the corresponding genetically encoded materials that they produce. DNA-directed protein expression and enzymatic mineralization occur on polystyrene microbeads in waterin-oil emulsions, yielding synthetic surrogates of biomineralizing cells that are then screened by flow sorting, with light-scattering signals used to sort the resulting mineralized composites differentially. We demonstrate the utility of this platform by evolutionarily selecting newly identified silicateins, biomineralizing enzymes previously identified from the silica skeleton of a marine sponge, for enzyme variants capable of synthesizing silicon dioxide (silica) or titanium dioxide (titania) composites. Mineral composites of intermediate strength are preferentially selected to remain intact for identification during cell sorting, and then to collapse postsorting to expose the encoding genes for enzymatic DNA amplification. Some of the newly selected silicatein variants catalyze the formation of crystalline silicates, whereas the parent silicateins lack this ability. The demonstrated bioengineered route to previously undescribed materials introduces in vitro enzyme selection as a viable strategy for mimicking genetic evolution of materials as it occurs in nature. directed evolution | in vitro compartmentalization | DNA shuffling | metal oxide nanoparticles | self-assembly

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Morphology of Sponge Spicules: Silicatein a Structural Protein for Bio‐Silica Formation

et al. 2010

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Japan) in consideration of his distinguished achievements in biomedicine. REVIEWMost forms of multicellular life have developed a calcium-based skeleton, while only a few specialized organisms complement their body plan with silica, such as sponges (phylum Porifera). However, the way in which sponges synthesize their silica is exceptional. They use an enzyme, silicatein, for the polymerization/polycondensation of silica, and thereby form their highly resistant and stabile massive siliceous skeletal elements (spicules). During this biomineralization process (i.e., biosilicification), hydrated amorphous silica is deposited within highly specialized sponge cells, ultimately resulting in structures that range in size from micrometers to meters. This peculiar phenomenon has been comprehensively studied in recent years and by several approaches; the molecular background was explored to create tools that might be employed for novel bio-inspired biotechnological and biomedical applications. Thus, it was discovered that spiculogenesis is mediated by the enzyme silicatein and starts intracellularly. The resulting silica nanoparticles fuse and subsequently form concentric lamellar layers around a central protein filament, consisting of silicatein and the scaffold protein silintaphin-1. Once the growing spicule is extruded into the extracellular space, it gains its final size and shape. Again, this process is mediated by silicatein and silintaphin-1, in combination with other molecules such as galectin and collagen. The molecular toolbox generated so far allows the fabrication of novel micro-and nanostructured composites, contributing to the economical and sustainable synthesis of biomaterials with unique characteristics.

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Crystalline Nanorods as Possible Templates for the Synthesis of Amorphous Biosilica during Spicule Formation in Demospongiae

Cited by 22 publications

References 34 publications

Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata

Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata

Evolutionary selection of enzymatically synthesized semiconductors from biomimetic mineralization vesicles

Morphology of Sponge Spicules: Silicatein a Structural Protein for Bio‐Silica Formation

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