Prescribing diatom morphology: toward genetic engineering of biological nanomaterials

Current Opinion in Chemical Biology

Volumn 11, Issue 6, 2007, Pages 662-669

  Kröger, Nils ^a  

^a Georgia Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NANOMATERIAL; POLYAMINE DERIVATIVE; SILICON DIOXIDE;

BIOGENESIS; BIOMINERALIZATION; CELL WALL; COMPLEX FORMATION; DIATOM; GENE FUNCTION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ENGINEERING; MOLECULAR MECHANICS; MORPHOLOGY; NONHUMAN; REVIEW; SCANNING ELECTRON MICROSCOPY; STRUCTURE ANALYSIS;

DIATOMS; GENETIC ENGINEERING; NANOSTRUCTURES; PEPTIDES; POLYAMINES; SILICON DIOXIDE;

BACILLARIOPHYTA; EUKARYOTA;

EID: 36549060585     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2007.10.009     Document Type: Review

References (41)

1. Field C.B., Behrenfeld M.J., Randerson J.T., and Falkowski P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281 (1998) 237-240
2. Round F.E., Mann D.G., and Crawford R.M. The Diatoms: Biology & Morphology of the Genera (1990), Cambridge University Press
3. Thamatrakoln K., Alverson A.J., and Hildebrand M. Comparative sequence analysis of diatom silicon transporters: toward a mechanistic model of silicon transport. J Phycol 42 (2006) 822-834
4. Thamatrakoln K., and Hildebrand M. Analysis of Thalassiosira pseudonana silicon transporters indicates distinct regulatory levels and transport activity through the cell cycle. Eukaryot Cell 6 (2007) 271-279
5. Sumper M., and Kröger N. Silica formation in diatoms: the function of long-chain polyamines and silaffins. J Mater Chem 14 (2004) 2059-2065
6. Armbrust E.V., Berges J.A., Bowler C., Green B.R., Martinez D., Putnam N.H., Zhou S., Allen A.E., Apt K.E., Bechner M., et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306 (2004) 79-86
7. Poulsen N., Chesley P.M., and Kröger N. Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 42 (2006) 1059-1065. This paper describes the first stable genetic transformation method for T. pseudonana, which exhibited the highest transformation efficiency for any diatom. The method uses microparticle bombardment to introduce the foreign DNA, and selection of transformants by resistance to the antibiotic nourseothricin. Two T. pseudonana expression vectors pTpfcp and pTpNR were developed that enabled constitutive expression and inducible expression, respectively, of introduced genes.
8. Poulsen N., and Kröger N. A new molecular tool for transgenic diatoms-control of mRNA and protein biosynthesis by an inducible promoter-terminator cassette. FEBS J 272 (2005) 3413-3423
9. Poulsen N., Berne C., Spain J., and Kröger N. Silica immobilization of an enzyme through genetic engineering of the diatom Thalassiosira pseudonana. Angew Chem Int Ed 46 (2007) 1843-1846. The work described in this paper established for the first time a method for the functionalization of nanopatterned silica structures using genetic engineering of diatoms. The method is based on expressing silaffin fusion proteins in transgenic T. pseudonana, which because of the presence of the silaffin domain leads to stable incorporation of the fusion protein into the forming silica in vivo. The method has been successfully applied for GFP and for the enzyme HabB. In both cases the activity of the protein was retained after isolation of the silica, and the stability of the protein was enhanced because of immobilization in the diatom silica.
10. Sumper M., and Brunner E. Learning from diatoms: nature's tools for the production of nanostructured silica. Adv Funct Mater 16 (2006) 17-26
11. Kröger N., and Poulsen N. Biochemistry and molecular genetics of silica biomineralization in diatoms. In: Baeuerelein E. (Ed). Handbook of Biomineralization Vol 1 (2007), Wiley-VCH, Weinheim 43-58
12. Kröger N., Deutzmann R., and Sumper M. Polycationic peptides from diatom biosilica that direct silica nanosphere formation. Science 286 (1999) 1129-1132
13. Kröger N., Deutzmann R., and Sumper M. Silica-precipitating peptides from diatoms: the chemical structure of silaffin-A from Cylindrotheca fusiformis. J Biol Chem 276 (2001) 26066-26070
14. Poulsen N., and Kröger N. Silica morphogenesis by alternative processing of silaffins in the diatom Thalassiosira pseudonana. J Biol Chem 279 (2004) 42993-42999
15. Wenzl S., Deutzmann R., Hett R., Hochmuth E., and Sumper M. Quaternary ammonium groups in silica-associated proteins. Angew Chem Int Ed 43 (2004) 5933-5936
16. Sumper M., Hett R., Lehmann G., and Wenzl S. A code for lysine modifications of a silica biomineralizing silaffin protein. Angew Chem Int Ed 46 (2007) 8405-8408. The authors described the chemical structures and positions within the polypeptide chain of the lysine residues in silaffin tpSil3. All except of 4 out of 33 lysine exhibited post-translational modifications, and the distribution of the different lysine derivatives exhibited a certain regularity. The authors speculate that the distribution pattern of the lysine derivatives within the tpSil3 polypeptide chain may contain information regarding silica morphogenesis.
17. Kröger N., Deutzmann R., Bergsdorf C., and Sumper M. Species-specific polyamines from diatoms control silica morphology. Proc Natl Acad Sci U S A 97 (2000) 14133-14138
18. Sumper M., Brunner E., and Lehmann G. Biomineralization in diatoms: characterization of novel polyamines associated with silica. FEBS Lett 579 (2005) 3765-3769
19. Sumper M., and Lehmann G. Silica pattern formation in diatoms: species-specific polyamine biosynthesis. ChemBioChem 9 (2006) 1419-1427
20. Brunner E., and Lutz K. Solid-state NMR in biomimetic silica formation and silica biomineralization. In: Behrens P., and Baeuerlein E. (Eds). Handbook of Biomineralization Vol 2 (2007), Wiley-VCH 19-38
21. Kröger N., and Sumper M. The molecular basis of diatom biosilica formation. In: Baeuerlein E. (Ed). Biomineralization. edn 2 (2004), Wiley-VCH 137-158
22. Poulsen N., Sumper M., and Kröger N. Biosilica formation in diatoms: Characterization of native silaffin-2 and its role in silica morphogenesis. Proc Natl Acad Sci U S A 100 (2003) 12075-12080
23. Sumper M. Biomimetic patterning of silica by long-chain polyamines. Angew Chem Int Ed 43 (2004) 2251-2254
24. Sumper M. A phase separation model for the nanopatterning of diatom biosilica. Science 295 (2002) 2430-2433
25. Pickett-Heaps J., Schmid A.M.M., and Edgar L.A. The cell biology of diatom valve formation. In: Round F.E., and Chapman D.J. (Eds). Progress in Phycological Research Vol 7 (1990), Bristol Biopress 1-169
26. van de Meene A.M.L., and Pickett-Heaps J.D. Valve morphogenesis in the centric diatom Proboscia alata Sundstrom. J Phycol 38 (2002) 351-363
27. Robinson D.H., and Sullivan C.W. How do diatoms make silicon biominerals?. TIBS 12 (1987) 151-154
28. Hildebrand M., Frigeri L.G., and Davis A.K. Synchronized growth of Thalassiosira pseudonana (Bacillariophyceae) provides novel insights into cell-wall synthesis processes in relation to the cell cycle. J Phycol 43 (2007) 730-740. In this paper, a method for the synchronization of cell wall development in T. pseudonana was described. The method was based on a silicic acid starvation-replenishment cycle. In the absence of silicic acid in the medium most cells got arrested at the early G1 phase, and upon replenishment of silicic acid progressed synchronously through one cell cycle. This synchronization method will greatly facilitate functional studies on the mechanism of silica formation, as well as other aspects of diatom biology.
29. Frigeri L.G., Radabaugh T.R., Haynes P.A., and Hildebrand M. Identification of proteins from a cell wall fraction of the diatom Thalassiosira pseudonana-insights into silica structure formation. Mol Cell Proteomics 5 (2006) 182-193. In this combined proteomics and genomics study the method for T. pseudonana cell cycle synchronization was employed to identify potential SDV associated proteins.
30. Knott J.M., Römer P., and Sumper M. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581 (2007) 3081-3086
31. Montsant A., Jabbari K., Maheswari U., and Bowler C. Comparative genomics of the pennate diatom Phaeodactylum tricornutum. Plant Phys 137 (2005) 500-513. On the basis of the complete of T. pseudonana genome sequence, extensive P. tricornutum EST data representing about half of the total number of genes and general gene database information comparative gene analyses were performed. This led to the identification of 1028 genes that appear to be diatom specific. Among those are probably a large number of genes involved in silica formation, and thus this analysis provides a starting point for functional analyses.
32. Walker T.L., Collet C., and Purton S. Algal transgenics in the genomic era. J Phycol 41 (2005) 1077-1093
33. Losic D., Rosengarten G., Mitchell J.G., and Voelcker N.H. Pore architecture of diatom frustules: potential nanostructured membranes for molecular particle separations. J Nanosci Nanotechnol 6 (2006) 982-989
34. Drum R.W., and Gordon R. Star Trek replicators and diatom nanotechnology. Trends Biotechnol 21 (2003) 325-328
35. Sandhage K.H., Allan S.M., Dickerson M.B., Ernst E.M., Gaddis C.S., Shian S., Weatherspoon M.R., Ahmad G., Cai Y., Haluska M.S., et al. Inorganic preforms of biological origin: Shape-preserving reactive conversion of biosilica microshells (diatoms). In: Behrens P., and Baeuerlein E. (Eds). Handbook of Biomineralization Vol 2 (2007), Wiley-VCH 235-253
36. Bao Z., Weatherspoon M.R., Shian S., Cai Y., Graham P.D., Allan S.M., Ahmad G., Dickerson M.B., Church B.C., Kang Z., et al. Chemical reduction of three-dimensional silica micro-assemblies into microporous silicon replicas. Nature 446 (2007) 172-175. This is the first demonstration of using the shape preserving inorganic conversion process to convert a nanopatterned amorphous silica structure (diatom silica) into crystalline silicon without compromising the nanomorphology. Owing to their high nanoporosity, the silicon replicas of diatom silica exhibit exceptional properties suitable for high-sensitivity, low-voltage gas sensing.
37. Lee S.J., Huang C.H., Shian S., and Sandhage K.H. Rapid hydrolysis of organophosphorous esters induced by nanostructured, fluorine-doped titania replicas of diatom frustules. J Am Ceram Soc 90 (2007) 1632-1636
38. 2 coatings on three-dimensional biosilica templates through hydroxyl group amplification and layer-by-layer alkoxide deposition. Angew Chem Int Ed 46 (2007) 5724-5727
39. Payne E.K., Rosi N.L., Xue C., and Mirkin C.A. Sacrificial biological templates for the formation of nanostructured metallic microshells. Angew Chem Int Ed 44 (2005) 5064-5067
40. Vrieling E.G., Sun Q., Tian M., Kooyman P., Gieskes W.W.C., van Santen R.A., and Sommerdijk N.A.J.M. Salinity-dependent diatom biosilicification implies an important role of external ion strength. Proc Natl Acad Sci U S A 104 (2007) 10441-10446. The work described in this paper demonstrated by using a variety of physical methods (SEM, AFM, BET analysis, SAXS, USAXS) that pore sizes and surface areas of diatom silica were significantly influenced by the salinity of the growth medium. Lower salinities lead to a decrease in pore size and surface area, which is in agreement with silica chemistry in vitro. The authors explained the observed effects by the fusion of endocytic vesicles with the SDV, which challenges the classical views of SDV development.
41. Matsunaga S., Sakai R., Jimbo M., and Kamiya H. Long-chain polyamines (LCPAs) from marine sponge: possible implication in spicule formation. ChemBioChem 8 (2007) 1729-1735. The authors described the isolation and structural characterization of LCPA from the sponge Axinyssa aculeata. They also demonstrated that the LCPA exhibit silica precipitation activity in vitro and induced the formation of aggregates of spherical particles. This was the first demonstration of the occurrence of LCPA in sponges and thus indicated that the mechanisms of silica formation in diatoms and sponges are much more closely related than previously assumed.