Coastal upwelling regions are among the most productive marine ecosystems but may be threatened by amplified ocean acidification. Increased acidification is hypothesized to reduce iron bioavailability for phytoplankton thereby expanding iron limitation and impacting primary production. Here we show from community to molecular levels that phytoplankton in an upwelling region respond to short-term acidification exposure with iron uptake pathways and strategies that reduce cellular iron demand. A combined physiological and multi-omics approach was applied to trace metal clean incubations that introduced 1200 ppm CO2 for up to four days. Although variable, molecular-level responses indicate a prioritization of iron uptake pathways that are less hindered by acidification and reductions in iron utilization. Growth, nutrient uptake, and community compositions remained largely unaffected suggesting that these mechanisms may confer short-term resistance to acidification; however, we speculate that cellular iron demand is only temporarily satisfied, and longer-term acidification exposure without increased iron inputs may result in increased iron stress.

• MeSH
• Ecosystem MeSH
• Phytoplankton * metabolism   MeSH
• Hydrogen-Ion Concentration MeSH
• Seawater * MeSH
• Iron metabolism   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH
• Names of Substances
• Iron MeSH

UNLABELLED: The model pennate diatom Phaeodactylum tricornutum is able to assimilate a range of iron sources. It therefore provides a platform to study different mechanisms of iron processing concomitantly in the same cell. In this study, we follow the localization of three iron starvation induced proteins (ISIPs) in vivo, driven by their native promoters and tagged by fluorophores in an engineered line of P. tricornutum. We find that the localization patterns of ISIPs are dynamic and variable depending on the overall iron status of the cell and the source of iron it is exposed to. Notwithstanding, a shared destination of the three ISIPs both under ferric iron and siderophore-bound iron supplementation is a globular compartment in the vicinity of the chloroplast. In a proteomic analysis, we identify that the cell engages endocytosis machinery involved in the vesicular trafficking as a response to siderophore molecules, even when these are not bound to iron. Our results suggest that there may be a direct vesicle traffic connection between the diatom cell membrane and the periplastidial compartment (PPC) that co-opts clathrin-mediated endocytosis and the "cytoplasm to vacuole" (Cvt) pathway, for proteins involved in iron assimilation. Proteomics data are available via ProteomeXchange with identifier PXD021172. HIGHLIGHT: The marine diatom P. tricornutum engages a vesicular network to traffic siderophores and phytotransferrin from the cell membrane directly to a putative iron processing site in the vicinity of the chloroplast.

• Keywords
• P. tricornutum, diatoms, fluorescent proteins, iron, iron starvation induced proteins, proteome, siderophores,
• Publication type
• Journal Article MeSH

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.

• Keywords
• Bigelowiella natans, iron, metagenomics, metatranscriptomics, photosynthesis, phytoplankton, proteomics,
• Publication type
• Journal Article MeSH