Light niche construction: Motility of sediment-inhabiting diatoms determines the experienced light environment

Abstract

Diatoms are an extraordinarily diverse, evolutionarily successful, and ecologically important group of single-cell algae. Diatoms of the group of the pennates are particularly important in estuarine sedimentary habitats, where they form highly productive microphytobenthos communities that cover extensive areas of intertidal flats. The pennates are capable of directed motility, an evolutionary and unique trait amongst diatoms, which has long been hypothesized to confer a critical adaptive advantage, by enabling these cells to vertically migrate within the photic zone of the sediment and behaviorally regulate light exposure. This study investigated the role of diatom motility on the active regulation of light exposure by developing a model to quantitatively characterize and compare the experienced light environment of individual cells of two life forms of pennate diatoms that inhabit intertidal estuarine sediments: epipelic species, motile cells dominant in fine sediments, and epipsammic species, non-motile or slowly motile cells, that colonize coarser sediments. The conceptual framework of the model was based on the identification and parameterization of the main controlling factors of the light regime perceived by cells inhabiting the two types of sedimentary environments: (i) solar irradiance incident at the sediment surface, determined by the superimposition of the tidal cycle on the day-night cycle; (ii) light attenuation within the sediment; (iii) sediment mixing by tidal currents or bioturbation, repositioning the cells in the sediment column; (iv) cell velocity, as a function of light intensity and of the photoacclimation state of the cells that determines their photosynthetic light preferences. The model was run for realistic scenarios based on published ecological, photophysiological and cellular motility data (light attenuation, mixing depth, photosynthesis light-response curves, cell velocity), simulating (i) the variation in the vertical position of a diatom cell due to vertical migration and (ii) the irradiance level to which it is exposed at each moment. The results confirm the hypothesis that epipelic and epipsammic diatoms experience a significantly different light environment. Vertical migration enables motile species to experience a much less variable light regime, with increased mean daily light doses received. In contrast, non-motile species experience a much more unstable light environment, including the frequent exposure to supersaturating light levels and to periods of prolonged darkness. These results have important ecological significance, as they support the adaptive value of light-driven motility as a form of optimizing photosynthesis and growth, and they identify vertical migration as a niche-construction activity, allowing motile diatoms to regulate the light environment they experience through habitat selection.