Predation is one of the strongest selection pressures phytoplankton has evolved strategies to cope with. Concurrently, phytoplankton growth must deal with resource acquisition. Experiments on mono- and mixed cultures of morphologically different diatoms exposed to copepods were performed to assess if size and shape were primary drivers in avoiding predation. Additionally, frustule silicification was investigated as a potential factor affecting prey selection by copepods. Thalassiosira pseudonana, Conticribra weissflogii, Cylindrotheca closterium, and Phaeodactylum tricornutum were exposed to the presence of Temora longicornis, a calanoid copepod. The physiological response in terms of growth, elemental composition and morphology was determined. The power of Image Flow Cytometry allowed functional single-cell analyses of mixed cultures in the presence and absence of copepods. Results highlighted that T. pseudonana although the most eaten by copepods in monospecific cultures, was not the preferred prey when the bigger C. weissflogii was added to the culture. When pennates were co-cultured with centric diatoms, their growth was unaffected by predators. Our data suggested that the frustule morphology contributes to long-term prey-predator interaction since the elongated thinner frustule, which evolved more recently, benefited cells in escaping from predators also when facing competition for resources.

In today’s oceans, diatoms are abundant and diverse primary producers distinguished by their silica shells. Although molecular clocks suggest that diatoms arose as much as 250 million years ago (Ma), the earliest known diatom fossils date from 190 Ma, leading to the suggestion that early diatoms were at best lightly silicified. By the Cretaceous Period, large circular (in cross section) diatoms with highly silicified frustules thrived in surface oceans, only later to be joined by species with elongated and thinner frustules, as well as lower SiO2 content. Decreased Si availability in surface oceans has been proposed as a principal driver of diatom evolution. Here, we investigate this through physiological experiments assessing the functional acclimation response of diatoms to reconstructed paleo-seawater. Four diatom species, differing in size and shape, were acclimated to reconstructed paleoenvironments mimicking Mesozoic/Cenozoic concentrations of nutrients in the presence of different Si regimes. When exposed to 500 µM Si, all populations, save for that of Conticribra weissflogii, became more highly silicified; the higher Si content per cell at 500 µM Si coincided with slower growth in small-sized cells. All species except C. weissflogii also showed lower photosynthetic efficiency as well as greater cell volume in comparison with diatoms acclimated to 205 or 25 µM Si. Average cell stoichiometry correlates with cell shape, but not size; pennates, in particular Phaeodactylum tricornutum, showed an acclimatory response to Si regimes, modulating Si use efficiency (the lower the external Si concentrations, the higher the C and N quotas per Si).Experimental data suggest that in the densely silicified and bigger C. weissflogii grown at higher Si, diffusion of silicic acid across membranes made a larger contribution to Si uptake, saving energy which could be reallocated into growth. In contrast, for less highly silicified and smaller species, high energy costs of Si homeostasis needed to prevent the overaccumulation of intracellular Si limited growth. While our experimental species reacted individualistically to changing silica availability, with distinct levels of plasticity, selective pressure associated with the temporal decline in Si availability may well have favored elongated shapes. Modern, less silicified species are unable to exploit high Si concentrations.

Diatoms represent the most abundant and diversified class of primary producers in present oceans; their distinctive trait is the ability to incorporate silicic acid in a silica outer shell called frustule. Numerous adaptative functions are ascribed to frustules, including the control of vertical movements through the water column; this indirectly determines cell access to fundamental resources such as light and nutrients, and favors diatom escape from predators. At the same time, light guides phototroph movements in the water column by affecting cell density (e.g., by modulating Si deposition in diatoms, vacuole volume, and/or solution). We investigated how the tremendous diversity in morphology and silicification that characterizes the frustule and the crucial role of light in diatom spatial distribution govern diatom sinking capacity. To test their integrative effects, we acclimated four diatoms distinguished by frustule traits (Chaetoceros muelleri, Conticribra weissflogii, Phaeodactylum tricornutum, and Cylindrotheca fusiformis) to different light conditions and evaluated their physiological performance in terms of growth, elemental composition, morphological changes, and their in vivo sinking capacity. What emerged from this study was that silicification, more than other morphological characteristics, controls species vertical movements, while a higher energy availability enhances cell floating independently from the silica content.

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