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Oct 21, 2008 - Diatoms, Biomineralization Processes, and Genomics. Mark Hildebrand*. Marine Biology Research Division, Scripps Institution of ...
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Chem. Rev. 2008, 108, 4855–4874

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Diatoms, Biomineralization Processes, and Genomics Mark Hildebrand* Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California 92093-0202 Received December 5, 2007

Contents 1. Introduction 1.1. Chemical Forms of Silicon 1.2. Diatoms as Biomineralizing OrganismssEvolutionary and Ecological Considerations 1.3. Diatom Cell Wall Features and Structure 1.4. Cell Cycle Aspects of Silicification 2. Transport and Intracellular Stabilization of Silicon 2.1. Chemical Forms of Silicon and Equilibrium Effects 2.1.1. The Intracellular Form of Silicon 2.2. General Characteristics of Diatom Silicon Transport 2.3. Molecular Characterization of Silicon Transport: The SITs 2.3.1. Mechanistic Models for SIT-Mediated Transport 2.4. Regulation of Silicic Acid Transport and the SITs 2.5. Kinetics- and Equilibrium-Based Model for Silicic Acid Transport 3. Silica Structure Formation 3.1. Silica Deposition Vesicle (SDV) 3.2. Definition of Three Scales of Structure Formation 3.3. Microscale Structure Formation 3.4. Nanoscale Structure Formation 3.5. Mesoscale Structure Formation 3.6. Integration of the Three Scales 4. Applications of Genomics, Proteomics, and Transcriptomics To Understand Diatom Silica Structure Formation 4.1. Genomics, Diatom Genome Sequencing 4.1.1. Thalassiosira pseudonana and Phaeodactylum tricornutum 4.1.2. Other Species in Progress and Future Genomic Approaches in Relation to Cell Wall Synthesis 4.2. Proteomics Approaches 4.3. Microarrays 4.4. Translational Regulation 4.5. Determining Protein Abundance and Intracellular Location 5. Genetic Manipulation Approaches To Understand Silica Cell Wall Formation 5.1. Diatom Transformation Systems

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* To whom correspondence should be addressed. Phone: (858) 822-0167. Fax: (858) 534-7313. E-mail: [email protected].

5.2. Controllable Promoters 5.3. Homologous Gene Replacement or Gene Downregulation 6. Technological Applications of Diatom Silica 7. Future Prospects 8. Acknowledgments 9. References

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1. Introduction Diatoms are eukaryotic unicellular microalgae with cell walls made of a composite of organic material, and silica which is often intricately and ornately shaped (Figure 1). Diatoms take up silicon from the environment in soluble form as silicic acid, transport it into the cell, and during the period of cell wall synthesis catalyze its polymerization into silica. A striking feature is the diversity of structures that diatoms make on the nano- to microscale (Figure 1), which is indicative of the molecular control of intracellular processes by which organics facilitate mineral formation. Diatom species are classified according to their cell wall structures, and the estimated number of species is at least in the tens of thousands and perhaps more.1,2 On a global scale, diatoms are the predominant contributors to biosilica formation in the oceans, which in total is estimated at 240 × 1012 mol per year.3 Diatoms have been a long-standing favorite of microscopists, and with the advent of electron microscopy came the ability to image at the nano- and microscale not only cell surface details by SEM but intracellular features by TEM. Two seminal publications in 1990, by Pickett-Heaps et al.4 and Round et al.,5 summarized detailed observationally-based models of diatom silicification. The work described in these reviews defined processes in formation of the mineral; however, molecular-level understanding of the organics involved was minimal. The rate of advance in the field slowed thereafter because of the time required to develop molecular approaches for diatoms. Because of the time delay, there was a discontinuity in the number of research groups in the field, and as a result, the earlier literature may not be completely assimilated by current researchers. For this reason, several aspects of this article will discuss new “discoveries” of which at least the general concepts were appreciated decades ago. It is hoped that the pioneers in the field understand the need for refreshing the concepts that they may have initially developed as newer researchers begin to experience them firsthand. It is also important to appreciate the validity of earlier work, which cannot be discounted just because molecular-level characterization was not possible at that time. Current-day models and concepts should fit within the wealth of observational data that was accumulated earlier. Examination of both macro- and molecular-scale

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Mark Hildebrand received his Ph.D. degree from the University of Arizona in 1987 and is currently a Research Scientist at the Scripps Institution of Oceanography, University of California, San Diego. His research is focused on diatoms, applying molecular, genomic, transgenic, and high-resolution imaging approaches to study formation of their nanostructured silica cell walls and understand mechanisms controlling carbon partitioning and lipid synthesis for biofuels production.

processes will be necessary to understand how diatoms form silica mineral structures that bridge nanometer to micrometer length scales using organic materials. The goal of this review is to provide an overview of diatom silicon metabolism and silica structure formation (including the use of genomics approaches), outline the potential for genetic manipulation of structure, and describe technological applications of diatom biosilica research.

1.1. Chemical Forms of Silicon Because of occasional confusion, it is useful to define terminology for the chemical forms of silicon that diatoms experience or produce. “Silicon” is the name of the elemental form and metal but is also used as a generic term to denote a silicon-containing compound whose precise chemical structure is unknown. The latter is especially important when describing soluble forms of silicon, which, for example, can exist in different polymerization states. Silicic acid, Si(OH)4, is the predominant soluble form at low concentrations (500 m g-1) and contained a significant population of micropores (e20 Å). The silicon replicas were photoluminescent and exhibited rapid changes in impedance upon exposure to gaseous nitric oxide, demonstrating their potential use as a gas sensor.173 Several of these types of materials demonstrate useful technological properties; a variety of nano- or microscale phosphors have been developed,173-175 highly sensitive gas sensors,170,173 and materials with useful catalytic properties such as degradation of organophosphorous esters found in insecticides and nerve agents.176 Continuing development of these approaches is likely to increase the variety of functional materials that can be derived from diatom silica, and optimize the ability to preserve structure. The approach of using a nanostructured biomineral as a template and converting its chemistry while maintaining structure has been termed the BaSIC (Bioclastic and Shape-preserving Inorganic Conversion) process.164 When coupled with the ability of diatoms to precisely replicate enormous numbers of structures, and the possibility of genetically tailoring diatom shape, these approaches represent a new paradigm in materials synthesis. The previous discussion dealt with techniques to modify the “final product” hard material of diatom frustules, but active research is ongoing to utilize the organics involved in diatom silica formation, and the living organism, to make functional materials. Two recombinant silaffins expressed and purified from E. coli were shown to form rutile (TiO2) at room temperature and neutral pH.177 An in vivo method of functionalizing diatom silica was recently published in which the bacterial enzyme hydroxylaminobenzene mutase (HabB) was genetically fused to a silaffin-derived targeting signal that enabled the enzyme to become incorporated into the silica of the living organism.139 Cleaned frustule material demonstrated HabB activity and stabilization to high temperature and organic solvents relative to the enzyme in solution.139 This is an exciting development because the system is self-contained by combining synthesis of the enzyme with its incorporation into the silica, which should minimize the cost of production.

7. Future Prospects In the past decade exciting developments have occurred in our understanding of diatom silica structure formation, including the first molecular-level characterization of the components involved,44,101,102 the first genetic manipulation,154 the first genome sequences and applications of related techniques,41,103,104 and most recently the development of diatoms as a source of nanoscale functional materials.139,164,177 With these initial footholds established and the availability of high-throughput analytical approaches, still coupled with the necessary detailed biochemical and molecular characterization, survey and comparative analyses along with genetic manipulation should provide the next level of insight.

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8. Acknowledgments The author is grateful to the people in the laboratory who contributed to this work, Kim Thamatrakoln, Aubrey Davis, Luciano Frigeri, Evelyn York, and Jessica Kelz and collaborators David Allison and Mitch Doktycz. Thanks to Andy Alverson for helpful discussions and references on diatom phylogeny. Special thanks to Nils Kro¨ger for critical reading of the manuscript and helpful comments. Research was supported by the Air Force Office of Scientific Research MURI grant RF00965521 and a grant from the Defense Advanced Research Projects Agency.

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