Nature's neat nanostructuration

Alexander M. Korsunsky, Phillip V. Sapozhnikov, Joris Everaerts, Alexei I. Salimon

Diatomic algae are an extensive class of single-cell marine and fluvial micro-organisms that build elaborately nano-structured hydrated silica exoskeletons. Diatoms have been an attractive topic in microscopy since 1850s, when their neat structures resolvable with the first widely affordable hobby microscopes drew the attention of an enthusiastic public. Diatoms are responsible for the production of around a quarter of all biomass and a quarter of all atmospheric oxygen on Earth, which highlights their indisputably important role in the planet’s ecology. Since 1990s diatoms have enjoyed renewed scientific interest as a source of biofuel, bioactive (anti-cancer) substances, and their possible use in photovoltaics and energy storage, nano-photonics, drug delivery, and other fields. Despite many decades of studies of the fascinating properties of diatomic frustules – electromagnetic, plasmonic, vibrational, and mechanical – such is the adaptability of diatoms to extreme conditions and the variety of diatomic species that many more questions persist.

Diatoms acquire their name from the predominantly asexual reproductive mechanism which involves cell division into two. An individual diatom grows by the extension of the girdle band that seals the gap between the two halves of the valve, one slightly larger (denoted epitheca) and one smaller (hypotheca). The cover image shows good contrast between the shiny epitheca at the top, and the matt girdle band on the side. Once the expansion of the girdle band (which itself consists of multiple pleural bands) results in the size of diatom sufficient for division, the growth of new silica valves begins within the diatom inside so-called Silica Deposition Vesicles (SDV’s), organelles enclosed by a lipid bilayer membrane (silicalemma) [1]. The growth is regulated through the activities of actin and tubulin proteins organized into microfilaments and microtubules, whose interaction determines the eventual nanostructure of the frustule.

Improved understanding of the detailed process of nanostructuration that occurs inside diatoms requires going beyond the superficial view shown in the cover image. Internal structure of diatoms and its evolution may be visualized either using non-destructive methods, such as fluorescent confocal microscopy [1], coherent X-ray ptychographic imaging [2], or destructive techniques, such as Focused Ion Beam sectioning [3].

The additional silicaceous parts needed to complete the new frustules are always built up inside the existing diatom. Hence, the frustule size in each next generation may reduce. Eventually, this reduction in size triggers rejuvenation accomplished by sexual reproduction, which restores the diatom size.

Despite decades of study of diatoms, great many questions persist regarding their structure and growth mechanisms. How does Nature control of the biosilication process result in the emergence of particular specific shapes and intricate patterns, such as the one shown in the cover image? What determines the large-scale properties, such as the overall symmetry of the frustule, and the fine structure, such as the nano-scale periodicity, as well as the small deviations from it, e.g. small adjustment of the overall size that is needed as a consequence of division? What drove the evolutionary selection of their shapes and structures, and how are they optimal for the conditions of diatom habitat? How are these growth algorithms coded in the diatom genome [4]? How can we ‘recruit’ to our advantage the natural process of low energy, large scale, large volume fabrication of structures with sub-100?nm features?

In our work to date, we have begun to address the connection between the structure and function of diatom frustules via the combination of electron microscopy and synchrotron X-ray methods, including imaging, diffraction, and spectroscopy. Aitken et al. [5] claim that Nature’s diatomic frustule design holds the record for specific structural bending strength. We use in-SEM nanoindentation of FIB-sectioned diatom frustule as unprecedented opportunity to observe their deformation response. Coupled with 3D modeling of the nanomechanics this will likely open new opportunities for improved nature-like structural design at small and large scales.

Diatoms, such as the Louboutensis Kolski (var. Diploneis interrupta), shown in the cover image display a degree of morphological variability, likely due to adaptation to the estuarine or littoral conditions. We explore this phenomenon by farming monocultured diatomic populations under controlled conditions on selected substrates, such as porous UHMWPE, PEEK, or silicon. Our observations reveal that diatom colonies adapt to the substrate with preferential attachment utilizing appropriately sized elements of relief [3].

Future research directions are likely to involve extrinsic approaches (control of ambient conditions, such as lighting, water salinity and ionic content, temperature, and agitation), as well as interventions in the intrinsic nature of algae, e.g. various mutagenic agents. As a consequence, the structure of diatomic frustules and colonies may be controlled across the hierarchy of characteristic lengths, from macroscopic to micrometer and nanometer scales.

Acknowledgment:

The authors wish to express their gratitude for the support provided under Royal Society grant IEC/R2/170223, EPSRC grant EP/P005381/1, and RFBR grant 18-44-920012.

Nature's neat nanostructuration

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