UV-shielding and wavelength conversion by centric diatom nanopatterned frustules

Abstract

Diatoms can represent the major component of phytoplankton and contribute massively to global primary production in the oceans. Over tens of millions of years they developed an intricate porous silica shell, the frustule, which ensures mechanical protection, sorting of nutrients from harmful agents, and optimization of light harvesting. Several groups of microalgae evolved different strategies of protection towards ultraviolet radiation (UVR), which is harmful for all living organisms mainly through the formation of dimeric photoproducts between adjacent pyrimidines in DNA. Even in presence of low concentrations of UV-absorbing compounds, several diatoms exhibit significant UVR tolerance. We here investigated the mechanisms involved in UVR screening by diatom silica investments focusing on single frustules of a planktonic centric diatom, Coscinodiscus wailesii, analyzing absorption by the silica matrix, diffraction by frustule ultrastructure and also UV conversion into photosynthetically active radiation exerted by nanostructured silica photoluminescence. We identified the defects and organic residuals incorporated in frustule silica matrix which mainly contribute to absorption; simulated and measured the spatial distribution of UVR transmitted by a single valve, finding that it is confined far away from the diatom valve itself; furthermore, we showed how UV-to-blue radiation conversion (which is particularly significant for photosynthetic productivity) is more efficient than other emission transitions in the visible spectral range.

Figure 1

Light micrographs of a living cell in face view (a) and side view (b); many small discoid chloroplasts are visible. FESEM micrographs of a cleaned single valve, inner view (c) and outer view of a complete theca (d). Scale bars: 50 μm.

Figure 2

Details of the inner (a) and external (b) plate of a single valve of C. wailesii diatom obtained by FESEM with progressive higher magnification. Scale bars: 10 μm (first row); 3 μm (second row); 1 μm (third row). The ultrastructure of the frustule, with pores of different dimensions, periodicity and lattice constant in different plates, is clearly visible. In particular, the ultrastructure of the outer plate is clearly visible through pores of the inner silica layer and vice versa.

Figure 3

Microscope images of a single valve at different distances from the lying plane for UVC (a, λ = 250 nm) and visible-near IR radiation (b, λ = 400–1100 nm).

Figure 4

Enhancement Factor (defined as the transmitted to incident intensity ratio) along the optical axis for different wavelengths. On right column, frontal views of the profiles are reported.

Figure 5

Raman spectra of a single valve of C. wailesii over the range 400–3200 cm⁻¹. The spectra were acquired in different points of the valve and then mediated. Blue spectra: mean over 22 spectra. Cyano spectra: mean over 3 spectra where presence of sulfur composites was detected. Complete band assignments are reported in Table 1.

Figure 6

Intensity spatial distribution in XZ plane of UV radiation transmitted by a single valve in air (left column); intensity profile of the first hot-spot with indication of its position along the optical z axis (right column). The simulations have been performed for λ = 250 nm (a), 280 nm (b) and 315 nm (c).

Figure 7

Intensity spatial distribution in the XZ plane of visible radiation transmitted by a single valve in air (left column); intensity profile of the first hot-spot with indication of its position along the optical z axis (right column). The simulations have been performed for λ = 460 nm (a), 532 nm (b) and 640 nm (c).

Figure 8

Intensity spatial distribution in the XZ plane of red radiation (λ = 640 nm) transmitted by a single valve embedded in the cytoplasm (left); intensity profile of the first hot-spot with indication of its position along the optical z axis (right).

Figure 9

Single valve of C. wailesii frustule emitting green radiation after excitation in 450–490 nm spectral range. The bright spots distributed over the valve are ascribable to organic residuals incorporated in the porous silica matrix of the frustule which are scarcely removable even after treatment with strong acid solutions. Scale bar: 50 μm (a). Photoluminescence spectra of C. wailesii valves after excitation at 325 (top) and 442 (down) nm. Incident power for excitation at 325 nm was 11.5 mW, while at 442 was 60 mW. In both cases, spectra have been acquired with an integration time of 1 second and then corrected respect to incident power (b).