Marine diatoms change their gene expression profile when exposed to microscale turbulence under nutrient replete conditions

Abstract

Diatoms are a fundamental microalgal phylum that thrives in turbulent environments. Despite several experimental and numerical studies, if and how diatoms may profit from turbulence is still an open question. One of the leading arguments is that turbulence favours nutrient uptake. Morphological features, such as the absence of flagella, the presence of a rigid exoskeleton and the micrometre size would support the possible passive but beneficial role of turbulence on diatoms. We demonstrate that in fact diatoms actively respond to turbulence in non-limiting nutrient conditions. TURBOGEN, a prototypic instrument to generate natural levels of microscale turbulence, was used to expose diatoms to the mechanical stimulus. Differential expression analyses, coupled with microscopy inspections, enabled us to study the morphological and transcriptional response of Chaetoceros decipiens to turbulence. Our target species responds to turbulence by activating energy storage pathways like fatty acid biosynthesis and by modifying its cell chain spectrum. Two other ecologically important species were examined and the occurrence of a morphological response was confirmed. These results challenge the view of phytoplankton as unsophisticated passive organisms.Oceanic plankton are characterised by a huge biodiversity spanning over many phyla. The different life strategies and behaviours displayed by such diverse organisms were selected also to cope with a patchy and variable 3D world driven by water motion 1 . Key factors for their survival, e.g., light availability, nutrient concentrations, prey abundance and water temperature, are all strongly tuned by the fluid motion at different scales. Fluid motion introduces kinetic energy in the system and turbulence is the way kinetic energy is transferred, through a dissipation cascade, over several eddy-like structures down to the smallest scale. Below this scale, energy is dissipated to heat via the friction of viscosity and water motion cannot prevail over molecular diffusion but can control it by changing local gradients 2, 3 . This is particularly important for unicellular phytoplankton which are surrounded by a fluid boundary layer where molecular diffusion is the dominant process and only solute (nutrient) chemical gradients assure cell provisioning. A distortion of the boundary layer would change these gradients, hence nutrients would diffuse more rapidly, enhancing the uptake rate 4 . For non-motile cells, like diatoms, the distortion of the boundary layer can be produced only by sinking or by the shear generated by the decay of turbulent kinetic energy. Therefore there is no more turbulence, as a random motion of water parcels, but the effects of turbulence which dissipates though sheared flow. Shear stress is what cells below Kolmogorov scale would ultimately perceive

Role of nutrient concentrations and water movement on diatom’s productivity in culture

“…Dell’Aquila and co-authors 42 hypothesized a better physiological state of cells grown under mixing compared to stagnant condition. Indeed, turbulence increases the chain length – used as proxy of a healthy physiological state 42 - of the diatom Chaetoceros decipiens , and induces energy storage pathways like fatty acid biosynthesis 51 .

Figure 3Cell concentration ( A) , cells mL −1 ) and PO 4 3− ( B ), SiO 4 4− ( C ), and NO 3 − ( D ) concentrations (µmol L −1 ) along the exponential growth phase in the original f/2 medium with water movement.

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Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence

“…When coupled with motility, turbulence can create patchiness in the distribution of phytoplankton at millimeter to centimeter scales (the Kolmogorov scale) (11,12), potentially impacting on populations' ecology by modulating cells' encounter rates and signaling. To cope with turbulence, phytoplankton can regulate lipid content, release of infochemicals, or gene expression profiles (13). On faster timescales, phytoplankton are able to respond to the fluid mechanical cues associated with turbulence (14) by regulating buoyancy (15) or switching migratory direction (16).…”

Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence

“…When coupled with motility, turbulence can create patchiness in the distribution of phytoplankton at millimeter to centimeter scales (the Kolmogorov length scale) ( 11 , 12 ), potentially impacting on population ecology by modulating cell encounter rates and signaling. To cope with turbulence, phytoplankton can regulate lipid content, release of infochemicals, or gene expression profiles ( 13 ). On behavioral timescales, phytoplankton are able to actively respond to the fluid mechanical cues associated with turbulence ( 14 ) by regulating buoyancy ( 15 ) or switching migratory direction—presumably to avoid turbulent patches—by rapidly modulating their cellular morphology ( 16 ).…”