Morphological and transcriptomic evidence for ammonium induction of sexual reproduction in Thalassiosira pseudonana and other centric diatoms

Abstract

The reproductive strategy of diatoms includes asexual and sexual phases, but in many species, including the model centric diatom Thalassiosira pseudonana, sexual reproduction has never been observed. Furthermore, the environmental factors that trigger sexual reproduction in diatoms are not understood. Although genome sequences of a few diatoms are available, little is known about the molecular basis for sexual reproduction. Here we show that ammonium reliably induces the key sexual morphologies, including oogonia, auxospores, and spermatogonia, in two strains of T. pseudonana, T. weissflogii, and Cyclotella cryptica. RNA sequencing revealed 1,274 genes whose expression patterns changed when T. pseudonana was induced into sexual reproduction by ammonium. Some of the induced genes are linked to meiosis or encode flagellar structures of heterokont and cryptophyte algae. The identification of ammonium as an environmental trigger suggests an unexpected link between diatom bloom dynamics and strategies for enhancing population genetic diversity.

Thoughts on the evolution and ecological niche of diatoms

“…It is noteworthy here that, in the experimentally triggered study on Thalassiosira pseudonana (Moore et al. 2017), sexual reproduction was accompanied by a high level of TEP production (K.H. Halsey, personal observation ).…”

“…If this is the case, then this advantage will be enhanced if sexual reproduction of a population is coordinated and especially if it is communicated or triggered once the population has achieved its critical density (Edlund and Stoermer 1997, Sterner and Elser 2002, Moore et al. 2017). Recently, it was shown that sexual division in the diatom, Thalassiosira pseudonana , can be experimentally triggered by high concentrations of ammonium, but only after reaching maximal cell density (Moore et al.…”

“…Recently, it was shown that sexual division in the diatom, Thalassiosira pseudonana , can be experimentally triggered by high concentrations of ammonium, but only after reaching maximal cell density (Moore et al. 2017). Chemically coordinated synchronization of sexual reproduction has also been indicated in other diatom species, along with the exudation of chemotaxic pheromones that may be involved in optimizing encounter rates between eggs and sperm (Koester et al.…”

Enhanced triacylglycerol (TAG) and protein accumulation in transgenic diatomThalassiosira pseudonanawith altered photosynthetic pigmentation

“…3), are both markers of stress. Under typical laboratory conditions, auxospore formation, which indicates sexual reproduction, is rarely if ever observed in T. pseudonana [Moore et al 2017]. In some diatom species, sexual reproduction serves as a way to reconstitute cell size, as it diminishes with every division.…”

“…pseudonana appears to maintain a relatively constant cell size. Sexual reproduction in diatoms may also be triggered by growth stress that leads to cell cycle arrest, such as nutrient depletion and oxidative stress [Moore et al 2017]. Because the LTL KD clones were grown in the same nutrient-replete media as WT, which did not form abundant auxospores, nutrient depletion is not a likely cause of the observed sexual reproduction in LTL KD clones.…”