Diatom of the Month – May 2018: Frustule optics related to photosynthesis in Coscinodiscus granii

by Johannes W. Goessling*

The centric diatom Coscinodiscus granii lives in coastal and pelagic marine habitats as a cosmopolitan phytoplanktonic species (algaebase.org). The genus name is derived from the greek words kóskino (sieve) and dískos (disc) and refers to the disc-shaped structure of the two valves that compose the silicate envelope (frustule) surrrounding diatoms. The valves of C. granii are perforated with pores and chambers in an outer layer with small pores (~10 nm), a central layer with hexagonal chambers (~1,200 nm), and an inner layer with large pores (~580 nm) (Fig. 1). So the size of these structures is only 1/100,000^th to 1/1000^th of a mm (!) and can therefore interact with the photons of sunlight. We were interested in the physical interaction of frustules with light, and how it can affect diatom photosynthesis – the conversion of sunlight into chemical energy. We found that the C. granii frustule redistributes sunlight to optimize the exposure of chloroplasts, i.e. the cellular organelles where photosynthesis takes place.

Fig. 1. A) Live cell of Coscinodiscus granii with evenly distributed chloroplasts (brownish rod-shaped structures). B) Scanninng electron micrograph of valves and girdle bands (ring-like silicate frustule structures that encircle the valves). C) Structurally different layers in the valve of C. granii in exploded scheme. The outer (top) layer  has small pores, the center has hexagonal chambers, and the inner side (bottom) is perforated with large pores. Images A and C by Johannes W. Goessling. Image B by Marianne Ellegaard.

Why some diatoms build such an interesting porous silicate structure around themselves has been debated for centuries. As relatively heavy parts compared to the cell, frustules may work as a ballast to sink rapidly when water column nutrients are low (Smetacek, 1985). The large pH buffering capacity of silicate could promote the enzymatic conversion of bicarbonate to carbon dioxide inside the cell and might thereby facilitate photosynthesis in aquatic environments (Milligan, 2002). Moreover, the highly ordered array of pores and chambers could protect the cell against the mandibles of copepods (through enormous mechanical resistance) thus reducing predation (Hamm et al., 2003); small pores can also keep harmful viruses and bacteria outside of the cell (Losic et al., 2006). Finally, the incident sunlight might be filtered for particular wavelengths through these highly ordered minuscule structures, thus affecting photosynthesis inside the living cell (Tommasi, 2016).

The diatom frustule has been described as a biological photonic crystal (Fuhrmann et al., 2004), a highly ordered, periodic structure, with dimensions matching the wavelength range of photons. Fuhrmann et al. suggested that C. granii valves can guide light in plane – a principle also known as photonic waveguiding that is used, for example, to transmit information through an optical fiber. To test this hypothesis in live diatoms, we used a microscopic technique to visualize photosynthesis in single cells (PAM chlorophyll fluorescence analyzer; Heinz Walz GmbH, Germany). When we focussed a laser beam only onto a small area of the living cell, the entire cell started to photosynthesize - even in chloroplasts located far away from the area of direct illumination (Goessling et al., 2018a). This was due to photonic waveguiding inside the silicate structure of the C. granii valve, while chloroplasts were apparently optically coupled to the electromagnetic field propagating inside the valve (Fig. 2). We further hypothesized that the asymmetric construction of the C. granii valve could increase the photosynthetically more productive radiation available inside the cell.

Fig. 2. Left: Chlorophyll fluorescence image of Coscinodiscus granii in false color code. Chlorophyll fluorescence emitted from chloroplasts is also recorded inside the silicate valve, suggesting coupling and transmittance of light between these two optical components. Right: Localized laser illumination induces photosynthesis all over the cell. Source: Goessling et al. 2018a.

When white light was sent onto the cell at certain angles of incidence, the frustule structures strongly enhanced blue light inside the cell (Fig. 3). The frustules of motile diatom species living in an intertidal mudflat, dominated by Gyrosigma sp., Staurophora sp. and Navicula spp., scattered and enhanced blue light by up to 120% , while blue light strongly attenuated inside the sediment where these species lived. These blue wavelengths (λ of ~440 nm) are preferentially absorbed by diatoms, because they contain more energy and support higher rates of photosynthesis (Goessling et al., 2016). We concluded that the optical properties of diatom frustules facilitate efficient photosynthesis in light limited environments (Goessling et al., 2018b).

Our future research will focus on the relationships between light availabilty in different habitats (benthic and pelagic), frustule optical properties of different species (such as raphid and phytoplanktonic species), and their photosynthetic activity.  We hypothesize that the frustule structure optimizes light harvesting of diatoms in relation to the light available in different habitats. The large structural diversity of frustules and associated optical properties could thereby also inspire innovation in the industrial technology sector, for example to optimize light harvesting and efficiencies of solar panels.

*Remote Sensing and Benthic Ecology Team, University of Nantes, France

References

Fuhrmann T, Landwehr S, El Rharbi-Kucki M, Sumper M. 2004. Diatoms as living photonic crystals. Applied Physics B: Lasers and Optics 78: 257–260.

Goessling JW, Cartaxana P, Kühl M. 2016. Photo-protection in the centric diatom Coscinodiscus granii is not controlled by chloroplast high-light avoidance movement. Frontiers in Marine Science 2: 1–10.

Goessling JW, Su Y, Cartaxana P, Maibohm C, Rickelt LF, Trampe ECL, Wangpraseurt D, Walby SL, Wu X, Ellegaard M, Kühl M. 2018a. Structure-based optics of centric diatom frustules: Modulation of the in vivo light field for efficient diatom photosynthesis. New Phytologist. 2018: 1-13.

Goessling JW, Frankenbach S, Ribeiro L, Serôdio J, Kühl M. 2018b. Valve optical properties of raphid diatoms and modulation of the light field: implications for niche differentiation in the microphytobenthos. Marine Ecology Progress Series 588: 29-42.

Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V. 2003. Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421: 841–843.

Losic D, Rosengarten G, Mitchell JG, Voelcker NH. 2006. Pore architecture of diatom frustules: potential nanostructured membranes for molecular and particle separations. Journal of nanoscience and nanotechnology 6: 982–989.

Milligan  a. J. 2002. A Proton Buffering Role for Silica in Diatoms. Science 297: 1848–1850.

Smetacek VS. 1985. Role of sinking in diatom life-hystory: ecological, evolutionary and geological significance. Marine Biology 84: 239–251.

Tommasi E De. 2016. Light manipulation by single cells: the case of diatoms. Journal of Spectroscopy 2016: 1–13.