Although sexual reproduction is believed to play a major role in the high diversification rates and species richness of diatoms, a mechanistic understanding of diatom life cycle control is virtually lacking. Diatom sexual signalling is controlled by a complex, yet largely unknown, pheromone system. Here, a sex-inducing pheromone (SIP+) of the benthic pennate diatom Seminavis robusta was identified by comparative metabolomics, subsequently purified, and physicochemically characterized. Transcriptome analysis revealed that SIP+ triggers the switch from mitosis-to-meiosis in the opposing mating type, coupled with the transcriptional induction of proline biosynthesis genes, and the release of the proline-derived attraction pheromone. The induction of cell cycle arrest by a pheromone, chemically distinct from the one used to attract the opposite mating type, highlights the existence of a sophisticated mechanism to increase chances of mate finding, while keeping the metabolic losses associated with the release of an attraction pheromone to a minimum.

Diatoms are species-rich microalgae that often have a unique life cycle with vegetative cell size reduction followed by size restoration through sexual reproduction of two mating types (MT(+) and MT(-)). In the marine benthic diatom Seminavis robusta, mate-finding is mediated by an L-proline-derived diketopiperazine, a pheromone produced by the attracting mating type (MT(-)). Here, we investigate the movement patterns of cells of the opposite mating type (MT(+)) exposed to a pheromone gradient, using video monitoring and statistical modeling. We report that cells of the migrating mating type (MT(+)) respond to pheromone gradients by simultaneous chemotaxis and chemokinesis. Changes in movement behavior enable MT(+) cells to locate the direction of the pheromone source and to maximize their encounter rate towards it.

Diatoms frequently dominate marine and freshwater biofilms as major primary producers. Nutrient resources in these biofilms are patchily distributed and fluctuate dynamically over time. We recently reported that this spatially and temporally structured environment can be exploited by motile diatoms that use chemoattraction to dissolved silicate (dSi) under Si starvation. Here, we show that the behavioral response of diatoms is more complex and selective as cells are also responding to gradients of dissolved phosphate (dP) when starved in this nutrient. In contrast, neither nitrate nor ammonium (dN) triggers an attractive response under nitrogen limitation. Video monitoring and movement pattern analysis of the model diatom Seminavis robusta revealed that dP attraction is mediated by a combined chemokinetic and chemotactic response. After locating nutrient hotspots, the microalgae slow down and recover from the limitation. The fastest recovery in terms of growth was observed after dSi limitation. In agreement with the lack of directional response, recovery from dN limitation was slowest, indicating that no short-term benefit would be drawn by the algae from the location of transient hotspots of this resource. Our results highlight the ability of diatoms to adapt to nutrient limitation by active foraging and might explain their success in patchy benthic environments.

Microorganisms encounter a diversity of chemical stimuli that trigger individual responses and influence population dynamics. However, microbial behavior under the influence of different incentives and microbial decision-making is poorly understood. Benthic marine diatoms that react to sexual attractants as well as to nutrient gradients face such multiple constraints. Here, we document and model behavioral complexity and context-sensitive responses of these motile unicellular algae to sex pheromones and the nutrient silicate. Throughout the life cycle of the model diatom Seminavis robusta nutrient-starved cells localize sources of silicate by combined chemokinetic and chemotactic motility. However, with an increasing need for sex to restore the initial cell size, a change in behavior favoring the attraction-pheromone-guided search for a mating partner takes place. When sex becomes inevitable to prevent cell death, safeguard mechanisms are abandoned, and cells prioritize the search for mating partners. Such selection processes help to explain biofilm organization and to understand species interactions in complex communities.