Ostreococcus tauri is a new model green alga for studying iron metabolism in eukaryotic phytoplankton

Abstract

BackgroundLow iron bioavailability is a common feature of ocean surface water and therefore micro-algae developed original strategies to optimize iron uptake and metabolism. The marine picoeukaryotic green alga Ostreococcus tauri is a very good model for studying physiological and genetic aspects of the adaptation of the green algal lineage to the marine environment: it has a very compact genome, is easy to culture in laboratory conditions, and can be genetically manipulated by efficient homologous recombination. In this study, we aimed at characterizing the mechanisms of iron assimilation in O. tauri by combining genetics and physiological tools. Specifically, we wanted to identify and functionally characterize groups of genes displaying tightly orchestrated temporal expression patterns following the exposure of cells to iron deprivation and day/night cycles, and to highlight unique features of iron metabolism in O. tauri, as compared to the freshwater model alga Chalamydomonas reinhardtii.ResultsWe used RNA sequencing to investigated the transcriptional responses to iron limitation in O. tauri and found that most of the genes involved in iron uptake and metabolism in O. tauri are regulated by day/night cycles, regardless of iron status. O. tauri lacks the classical components of a reductive iron uptake system, and has no obvious iron regulon. Iron uptake appears to be copper-independent, but is regulated by zinc. Conversely, iron deprivation resulted in the transcriptional activation of numerous genes encoding zinc-containing regulation factors. Iron uptake is likely mediated by a ZIP-family protein (Ot-Irt1) and by a new Fea1-related protein (Ot-Fea1) containing duplicated Fea1 domains. The adaptation of cells to iron limitation involved an iron-sparing response tightly coordinated with diurnal cycles to optimize cell functions and synchronize these functions with the day/night redistribution of iron orchestrated by ferritin, and a stress response based on the induction of thioredoxin-like proteins, of peroxiredoxin and of tesmin-like methallothionein rather than ascorbate. We briefly surveyed the metabolic remodeling resulting from iron deprivation.ConclusionsThe mechanisms of iron uptake and utilization by O. tauri differ fundamentally from those described in C. reinhardtii. We propose this species as a new model for investigation of iron metabolism in marine microalgae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2666-6) contains supplementary material, which is available to authorized users.

Marine Prasinoviruses and Their Tiny Plankton Hosts: A Review

“…Three clades of Ostreococcus —A, C and D—are classified as high-light adapted, as defined through laboratory photophysiology assessments, and clade B is described as low-light adapted [40]. However, this low-light adapted clade has been reported in surface waters [8,43] and although different ecotypes do not commonly occur at the same geographical location, the drivers behind clade distribution may be more complex than determined by sea surface irradiance levels alone [43]. The putative low-light ecotype strain has increased photosensitivity and an adapted photoprotection mechanism.…”

“…TEM analysis confirmed viruses are localised to a region of the cytoplasm and do not associate with the nucleus or other organelles [30]. Ostreococcus and their viruses are globally distributed in coastal and open-ocean euphotic environments [34,36,43]. Viruses that infect O. tauri have been reported to be prevalent in coastal sites [32,33,36], whilst OlVs have been detected in more widespread marine locations, including oligotrophic sites in the Atlantic and Pacific Oceans [34,36,71,72], although this geographical distribution is not related to genetic distance, based on analysis of the polB gene [36].…”

Regulating cellular trace metal economy in algae

“…These transporters belong to a mix of protein families with origins in various lineages and unique phylogenetic occurrences (Figure 2). For instance, Fe uptake at the plasma membrane occurs by a reduction-oxidation-transport mechanism, involving FRE1 (Fe reductase), FOX1 (Fe oxidase) and FTR1 (permease) [15–19], which is found in other algae, such as rhodophytes and diatoms [20], but absent from most land plants and prasinophytes [21,22] (Figure 2A). Additional components of high-affinity Fe uptake include the soluble secreted proteins FEA1 and FEA2, which are only found in the algal lineages [17,23,24].…”

“…Instead of Fe-storage, these ferritins are proposed to mediate an Fe-sparing/recycling process involving degradation of the Fe-rich photosystem I (PSI) complex [37]. The Ostreococcus tauri ferritin appears to play a similar role in buffering Fe in the chloroplast (rather than storage) as a function of the day/night cycle [22,38]. Although ferritin is central to iron homeostasis in both green algae and diatoms [39], it is not found in all algal genomes (Figure 4B).…”

Acclimation of a low iron adapted Ostreococcus strain to iron limitation through cell biomass lowering

“…We recently unveiled a central role for ferritin in the day-night regulation of iron homeostasis in the picoeukaryotic alga Ostreococcu s tauri and showed that the transcriptional response to iron limitation in this microorganism is tighly dependent on the diurnal cycle 17, 18 . Still, the adaptive responses of eukaryotic picophytoplankton to low iron conditions remain largely unexplored.…”