Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

Abstract

Summary Microalgae play a major role as primary producers in aquatic ecosystems. Cell signalling regulates their interactions with the environment and other organisms, yet this process in phytoplankton is poorly defined. Using the marine planktonic diatom Pseudo‐nitzschia multistriata, we investigated the cell response to cues released during sexual reproduction, an event that demands strong regulatory mechanisms and impacts on population dynamics.We sequenced the genome of P. multistriata and performed phylogenomic and transcriptomic analyses, which allowed the definition of gene gains and losses, horizontal gene transfers, conservation and evolutionary rate of sex‐related genes. We also identified a small number of conserved noncoding elements.Sexual reproduction impacted on cell cycle progression and induced an asymmetric response of the opposite mating types. G protein‐coupled receptors and cyclic guanosine monophosphate (cGMP) are implicated in the response to sexual cues, which overall entails a modulation of cell cycle, meiosis‐related and nutrient transporter genes, suggesting a fine control of nutrient uptake even under nutrient‐replete conditions.The controllable life cycle and the genome sequence of P. multistriata allow the reconstruction of changes occurring in diatoms in a key phase of their life cycle, providing hints on the evolution and putative function of their genes and empowering studies on sexual reproduction.

Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)

“…Rapheenabled motility relies on an actin-myosin system (Poulsen et al, 1999), and is directional, reversible and much faster than other forms of movement present in some nonraphid diatoms (Pickett-Heaps et al, 1986, 1991Kooistra et al, 2003). Active motility in vegetative cells enabled directed movement towards microhabitats with specific light, nutrient and temperature conditions (Cohn et al, 2015;Bondoc et al, 2016a), diurnal and tidal migrations (Palmer & Round, 1967), gravitactic behaviors (Frankenbach et al, 2014), predator avoidance (Kingston, 1999) and pheromonal migration (Sato et al, 2011;Gillard et al, 2013;Bondoc et al, 2016b;Moeys et al, 2016;Basu et al, 2017). This broad range of ecological benefitsunavailable to nonraphid diatomsexpanded the repertoire of habitats available for colonization, creating new opportunities for niche specialization.…”

Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom

“…We identified dab genes with the same genetic organization and high sequence identity in the genome of the known DA-producing Pseudo-nitzschia multistriata (fig. S17) (30). Moreover, of the eight publicly available Pseudo-nitzschia transcriptomes, only the highly toxic DA-producing species Pseudo-nitzschia australis expressed the dab genes (figs.…”

Colin Brownlee

“…Basu et al . () address this knowledge gap by identifying genes specifically involved in the sexual life cycle phase, opening new avenues for study of this important process. While the global importance of phytoplankton is undisputed, the limitations of phytoplankton growth are still poorly understood.…”