Bionic 3D printed corals

Abstract

Corals have evolved as optimized photon augmentation systems, leading to space-efficient microalgal growth and outstanding photosynthetic quantum efficiencies. Light attenuation due to algal self-shading is a key limiting factor for the upscaling of microalgal cultivation. Coral-inspired light management systems could overcome this limitation and facilitate scalable bioenergy and bioproduct generation. Here, we develop 3D printed bionic corals capable of growing microalgae with high spatial cell densities of up to 10⁹ cells mL^-1. The hybrid photosynthetic biomaterials are produced with a 3D bioprinting platform which mimics morphological features of living coral tissue and the underlying skeleton with micron resolution, including their optical and mechanical properties. The programmable synthetic microenvironment thus allows for replicating both structural and functional traits of the coral-algal symbiosis. Our work defines a class of bionic materials that is capable of interacting with living organisms and can be exploited for applied coral reef research and photobioreactor design.

Fig. 1. Structure of natural and 3D printed bionic corals.

Colony of the coral Stylophora pistilla growing at about 10 m depth on Watakobi Reef, East Sulawesi, Indonesia (a). Close-up photograph (b, c) and optical coherence tomography scanning (d, e) of coral skeleton and coral tissue, respectively. Scanning electron microscopy image of successful 3D printed skeleton replica showing corallites in 1:1 scale relative to the original design (f). Photograph of living bionic coral growing Symbiodinium sp. microalgae (g). The living tissue was printed on top of the skeleton mimic and the bionic coral was cultured for 7 days. Scale bar = 1 mm (b–f) and 750 µm (g).

Fig. 2. Optical properties of 3D printed bionic coral tissue and skeleton.

3D rendering of final bionic coral design (a). Bionic skeletal design optimization (b–d) showing SEM images of the original Stylophora pistillata corallite architecture (scale bar = 200 µm) (b), a 3D printed intermediate skeleton design (scale bar = 300 µm) (c) and the final bionic skeleton doped with CNC aggregates (scale bar = 100 µm) (d). 3D tetrahedral mesh-based Monte Carlo simulation (e–g). Light (675 nm) is irradiated over the connecting tissue (red arrow) as a collimated pencil beam. The time-resolved solution of photon migration (temporal point spread function, TPSF [1/mm³]) is shown after 0.5 ns (left column), 3 ns (center column), and 4.5 ns (right column) in a cross-cut view of the 2-layer bionic coral (e), a 1-layer bionic tissue (f) and non-scattering GelMA (g). The microalgal density in the tissue component is identical for all simulations (µ_a = 15 mm⁻¹). The angular distribution of forward scattered light (θ = 270°–90°) at 550 nm is shown as normalized transmittance (h). Microprobe-based fluence rate measurements (E₀ in % of incident irradiance) for the bionic coral (i) and a flat slab of GelMA (j) both with a microalgal density of 5.0 × 10⁶ cells mL⁻¹.

Fig. 3. Performance testing of 3D printed bionic coral.

Growth of Marinichlorella kaistiae KAS603 in bionic coral (a). Data are means ( ± SEM, n = 3-6 bionic coral prints). Dark and bright red areas show 95% confidence and prediction intervals, respectively. Vertical attenuation of fluence rate (E₀ at 675 nm) at the beginning (day 1, means ± SEM, n = 4) and end of the performance test (day 12, means ± SEM, n = 3) (b). Net photosynthetic rates at day 5, 8, and 11 (means ± SEM, n = 3–10 corallites) (c). Lines represent curve fits (see Methods). Gross photosynthetic rates at day 5 (black) and day 8 (blue) (d). Symbols are means (±SEM, n = 2–6 corallites), lines are curve fits. Measurements were performed with O₂ microsensors at the center of the corallite cup surface (closed symbols/solid lines) and at a vertical depth of 300 µm (open symbols/dashed lines).

Fig. 4. Living 3D printed bionic coral.

Horizontal view of 7-day old bioprinted construct, showing aggregates of the green microalga Marinichlorella kaistiae KAS603 (scale bar = 100 µm) (a). Maximum z projection of confocal images showing chlorophyll a fluorescence of bionic tentacles (scale bar = 50 µm) (b) and a M. kaistiae KAS603 aggregate (scale bar = 20 µm) (c). SEM image of bionic tissue showing porous tissue scaffolds (scale bar = 20 µm) (d) and a close-up of a microalgal aggregate (scale bar = 10 µm) (e).