Copper and iron metabolism in <i>Ostreococcus tauri</i> – the role of phytotransferrin, plastocyanin and a chloroplast copper-transporting ATPase

Scheiber, Ivo F.; Pilátová, Jana; Malych, Ronald; Kotabová, Eva; Krijt, Matyáš; Vyoral, Daniel; Mach, Jan; Léger, Thibaut; Camadro, Jean‐Michel; Prášil, Ondřej; Lesuisse, Emmanuel; Šuták, Robert

doi:10.1039/c9mt00078j

Cited by 19 publications

(10 citation statements)

References 40 publications

(71 reference statements)

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“…Not surprisingly, among the proteins most dramatically regulated by iron were two homologues of the Fea1-domain-containing proteins functioning as phytotransferrins, experimentally verified to be responsible for iron utilization in the diatom Phaeodactylum tricornutum (iron starvation-induced protein Isip2a) (6, 7) and the picoalga Ostreococcus tauri (Ot-FEA1) (27,28). The expression of both proteins dropped 2-fold 6 h after iron supplementation, and the changes reached 8.7-fold and 10.8-fold, respectively, after 24 h. A similar decrease in abundance was observed for a member of the COG0523 family of putative metal chaperones (29,30) with known functions in binding and trafficking of metals (Zn, Co, and Fe) to various cellular processes.…”

Section: Resultsmentioning

confidence: 99%

Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability

et al. 2021

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The productivity of the ocean is largely dependent on iron availability, and marine phytoplankton have evolved sophisticated mechanisms to cope with chronically low iron levels in vast regions of the open ocean. By analyzing the metabarcoding data generated from the Tara Oceans expedition, we determined how the global distribution of the model marine chlorarachniophyte Bigelowiella natans varies across regions with different iron concentrations. We performed a comprehensive proteomics analysis of the molecular mechanisms underpinning the adaptation of B. natans to iron scarcity and report on the temporal response of cells to iron enrichment. Our results highlight the role of phytotransferrin in iron homeostasis and indicate the involvement of CREG1 protein in the response to iron availability. Analysis of the Tara Oceans metagenomes and metatranscriptomes also points to a similar role for CREG1, which is found to be widely distributed among marine plankton but to show a strong bias in gene and transcript abundance toward iron-deficient regions. Our analyses allowed us to define a new subfamily of the CobW domain-containing COG0523 putative metal chaperones which are involved in iron metabolism and are restricted to only a few phytoplankton lineages in addition to B. natans. At the physiological level, we elucidated the mechanisms allowing a fast recovery of PSII photochemistry after resupply of iron. Collectively, our study demonstrates that B. natans is well adapted to dynamically respond to a changing iron environment and suggests that CREG1 and COG0523 are important components of iron homeostasis in B. natans and other phytoplankton. IMPORTANCE Despite low iron availability in the ocean, marine phytoplankton require considerable amounts of iron for their growth and proliferation. While there is a constantly growing knowledge of iron uptake and its role in the cellular processes of the most abundant marine photosynthetic groups, there are still largely overlooked branches of the eukaryotic tree of life, such as the chlorarachniophytes. In the present work, we focused on the model chlorarachniophyte Bigelowiella natans, integrating physiological and proteomic analyses in culture conditions with the mining of omics data generated by the Tara Oceans expedition. We provide unique insight into the complex responses of B. natans to iron availability, including novel links to iron metabolism conserved in other phytoplankton lineages.

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Section: Resultsmentioning

confidence: 99%

Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability

et al. 2021

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“…The Ot-Fea1 protein contains several motifs thought to play a key role in iron transport by fungal Ftr1 proteins (Fang and Wang, 2002) -R/K-E/D-X-X-E and R/K-E-X-X-E/D -and it has been shown experimentally to bind iron (Lelandais et al, 2016). Its expression was modulated by Zn, and the protein was purified in association with ferric iron (Scheiber et al, 2019). A phylogeny of homologous Fea1 and Isip2a domains from algal proteins showed this protein to be widespread in different algal groups, with multiplication of the Fea1 domain clearly having occurred on several independent occasions (Lelandais et al, 2016).…”

Section: Ostreococcus Tauri As a Model Organism For Studying Iron Uptmentioning

confidence: 99%

Iron Uptake Mechanisms in Marine Phytoplankton

2020

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Oceanic phytoplankton species have highly efficient mechanisms of iron acquisition, as they can take up iron from environments in which it is present at subnanomolar concentrations. In eukaryotes, three main models were proposed for iron transport into the cells by first studying the kinetics of iron uptake in different algal species and then, more recently, by using modern biological techniques on the model diatom Phaeodactylum tricornutum. In the first model, the rate of uptake is dependent on the concentration of unchelated Fe species, and is thus limited thermodynamically. Iron is transported by endocytosis after carbonate-dependent binding of Fe(III)' (inorganic soluble ferric species) to phytotransferrin at the cell surface. In this strategy the cells are able to take up iron from very low iron concentration. In an alternative model, kinetically limited for iron acquisition, the extracellular reduction of all iron species (including Fe') is a prerequisite for iron acquisition. This strategy allows the cells to take up iron from a great variety of ferric species. In a third model, hydroxamate siderophores can be transported by endocytosis (dependent on ISIP1) after binding to the FBP1 protein, and iron is released from the siderophores by FRE2-dependent reduction. In prokaryotes, one mechanism of iron uptake is based on the use of siderophores excreted by the cells. Iron-loaded siderophores are transported across the cell outer membrane via a TonB-dependent transporter (TBDT), and are then transported into the cells by an ABC transporter. Open ocean cyanobacteria do not excrete siderophores but can probably use siderophores produced by other organisms. In an alternative model, inorganic ferric species are transported through the outer membrane by TBDT or by porins, and are taken up by the ABC transporter system FutABC. Alternatively, ferric iron of the periplasmic space can be reduced by the alternative respiratory terminal oxidase (ARTO) and the ferrous ions can be transported by divalent metal transporters (FeoB or ZIP). After reoxidation, iron can be taken up by the high-affinity permease Ftr1.

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“…For proteins identified only in one of the conditions, intensity of 23 was selected as a lowest value to be included, on basis of previous imputation experience. To distinguish significantly downregulated or upregulated proteins in the iron-deficient conditions in S1 and S2 Tables, the threshold of fold change >2.3 and <-2.3 was chosen, based on previous experience and published results on comparative proteomics in N. gruberi and Ostreococcus tauri [34,54].…”

Section: Comparative Proteomic Analysismentioning

confidence: 99%

Adaptive iron utilization compensates for the lack of an inducible uptake system in Naegleria fowleri and represents a potential target for therapeutic intervention

et al. 2020

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Naegleria fowleri is a single-cell organism living in warm freshwater that can become a deadly human pathogen known as a brain-eating amoeba. The condition caused by N. fowleri, primary amoebic meningoencephalitis, is usually a fatal infection of the brain with rapid and severe onset. Iron is a common element on earth and a crucial cofactor for all living organisms. However, its bioavailable form can be scarce in certain niches, where it becomes a factor that limits growth. To obtain iron, many pathogens use different machineries to exploit an iron-withholding strategy that has evolved in mammals and is important to host-parasite interactions. The present study demonstrates the importance of iron in the biology of N. fowleri and explores the plausibility of exploiting iron as a potential target for therapeutic intervention. We used different biochemical and analytical methods to explore the effect of decreased iron availability on the cellular processes of the amoeba. We show that, under iron starvation, nonessential, iron-dependent, mostly cytosolic pathways in N. fowleri are downregulated, while the metal is utilized in the mitochondria to maintain vital respiratory processes. Surprisingly, N. fowleri fails to respond to acute shortages of iron by inducing the reductive iron uptake system that seems to be the main iron-obtaining strategy of the parasite. Our findings suggest that iron restriction may be used to slow the progression of infection, which may make the difference between life and death for patients.

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Copper and iron metabolism in Ostreococcus tauri – the role of phytotransferrin, plastocyanin and a chloroplast copper-transporting ATPase

Abstract: We have identified Ostreococcus tauri major iron uptake mediating protein, phytotransferrin (Ot-FEA1), whose expression and binding of iron is copper dependent.

Cited by 19 publications

References 40 publications

Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability

Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability

Iron Uptake Mechanisms in Marine Phytoplankton

Adaptive iron utilization compensates for the lack of an inducible uptake system in Naegleria fowleri and represents a potential target for therapeutic intervention

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