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Kröger Group - Biomineralization

Biomineralization

The formation of inorganic materials with complex form is a widespread biological phenomenon (biomineralization) that occurs in almost all groups of organisms from prokaryotes (e.g., magnetite nanocrystals in certain bacteria) to humans (bone and teeth). Among the most spectacular examples of biomineralization are the intricately structured cell walls of diatoms, a large group of single-celled eukaryotic algae that are present in almost all water habitats. Diatom cell walls are made of amorphous, hydrated SiO2 (silica) and exhibit highly regular porous patterns (Figure 1).


Figure 1. Structure of diatom cell walls. Secondary electron microscopy (SEM) images of overviews (top row) and details (bottom row) of the cell walls from four different diatom species (taken from reference 11)

The complex biomineral structures of diatoms illustrate our limited understanding of a very fundamental biological question: How does a cell translate DNA sequence information into a patterned three-dimensional structure? There are tens of thousands diatom species, each forming a different aesthetically sculptured silica cell wall withcharacteristic nano- and micropatterns (Figure 1). Diatoms have thus mastered the combination of two contradictory capabilities: the biosynthesis of complex structures with high fidelity, and the seemingly infinite variation of this process. Therefore, important lessons can be learned from diatoms regarding the mechanism by which eukaryotic cells assemble the cellular machinery to execute a morphogenetic program.

Diatom silica is produced from Si(OH)4 (orthosilicic acid), which is taken up into the cell by specific transporter proteins (SITs). By a yet unidentified pathway, the silicic acid is concentrated and stored inside the cell until it polymerized into silica inside specific intracellular compartments, the silica deposition vesicles (SDVs) (Figure 2).


Figure 2. Schematic structure of the diatom cell (center) and diatom cell cycle.10 Diatom cells are shown in cross section. The gray area represents the protoplast, the green line depicts the plasma membrane. For simplicity, intracellular organelles other than the silica deposition vesicle (SDV) are not shown. Cells arranged in the circle show different stages of the cell cycle: (1) Shortly before cell division the cell wall contains the maximum number of girdle bands; (2) immediately after cytokinesis new biosilica (red ) is formed in each sibling cell inside a valve SDV ( yellow); (3) expansion of the valve SDVs as more and more silica is deposited; (4) at the final stage of valve SDV development, each SDV contains a fully developed valve; (5) the newly formed valves are deposited in the cleavage furrow on the surface of each protoplast by SDV exocytosis; (6) the sibling cells have separated; (7+8) expansion of the protoplast in interphase requires the synthesis of new silica (red ) inside girdle band SDVs (yellow); each girdle band is synthesized in a separate SDV, and after SDV exocytosis is added to the newly formed valve (hypovalve); (9) after synthesis of the final hypovalve girdle band (pleural band) cell expansion stops, and DNA replication is initiated.

The aim of the Kröger group is to understand the mechanism of silica formation in diatoms to discover fundamental principles of biomineral morphogenesis. We approach this task using experimental tools from biochemistry, molecular genetics, and molecular cell biology. The work involves identification of the morphogenetic biomolecules, investigation of their properties in vitro, and studies on their influence on silica biogenesis in vivo. Previously work by the Kröger group and others have led to the identification of highly unusual proteins (silaffins1-5, cingulins6, silacidins7,8) and long-chain polyamines (LCPA)9 that are intimately associated with diatom biosilica, and are believed to be directly involved in its morphogenesis (Figure 3).


Figure 3. Structure of biomolecules involved in diatom silica formation. Chemical structures of (A) the silaffin peptide natSil-1A1, and (B) long-chain polyamines (LCPA).

Current activities in the Kröger group are directed towards (i) understanding the interplay between the known silica forming components, (ii) determining the role of each component in silica morphogenesis in vivo, and (iii) identifying the complete set of biomolecules involved in diatom silica formation.

Insight into the mechanisms of biomineralization in diatoms is not only interesting from a biological point of view. Over the past decade the discovery of fundamental principles of this process has spurred biomimetic and bioenabled methods for the production of nanopatterned functional ceramics under mild reaction conditions. The Kröger is also actively involved in this research field (see Bionanotechnology).

References

  1. N. Kröger, R. Deutzmann, M. Sumper (1999) Science 286, 1129-32.
  2. N. Kröger, R. Deutzmann, M. Sumper (2001) J. Biol. Chem. 276, 26066-70.
  3. N. Kröger, S. Lorenz, E. Brunner, M. Sumper (2002) Science 298, 584-6.
  4. N. Poulsen, M. Sumper, N. Kröger (2003) Proc. Natl. Acad. Sci. USA 100, 12075-80. 
  5. N. Poulsen, N. Kröger (2004) J. Biol. Chem. 279, 42993-9.
  6. A. Scheffel, N. Poulsen, S. Shian, N. Kröger (2011) Proc. Natl. Acad. Sci. USA 108, 3175-3180.  
  7. S. Wenzl, R. Hett, P. Richthammer, M. Sumper (2008) Angew. Chem. Int. Ed. 47, 1729-32  
  8. P. Richthammer, M Börmel, E. Brunner, K.-H. van Pee (2011) ChemBioChem 12, 1362-6.
  9. N. Kröger, R. Deutzmann, C. Bergsdorf, M. Sumper (2000) Proc. Natl. Acad. Sci. USA 97, 14133-8.
  10. N. Kröger, N. Poulsen, (2008) Annu. Rev. Genet. 42, 83-107.
  11. F. E. Round, D. G. Mann, R. M. Crawford, The Diatoms: Biology & Morphology of the Genera. Cambridge Univ. Press (1990).