Sarah Rose Smith

The Intergovernmental Panel on Climate Change (IPCC) has clearly stated that carbon dioxide removal (CDR) must happen in parallel with CO2 emissions reductions, and the giga-tonne scale of CDR that is needed will only become a reality if storage in the oceans is seriously considered. One such marine CDR (mCDR) approach is ocean iron fertilization (OIF), which harnesses carbon drawdown by phytoplankton in areas of the ocean where growth is limited by iron availability. A new generation is poised to build on the rich history of prior OIF research with parallel objectives of i) addressing knowledge gaps and uncertainties regarding the additionality and durability of OIF mCDR; and ii) fully evaluating the ecological and environmental impacts of iron addition. To ensure these new field trials are carried out in a transparent and responsible manner with the appropriate guardrails, they must be developed and conducted in collaboration with social scientists, governance experts, and in consultation with interested communities. The Exploring Ocean Iron Solutions (ExOIS) consortium is a multidisciplinary group of researchers focused on exploring OIF through natural science, social science, and governance lenses to contribute to our growing understanding of how mCDR may be responsibly used to combat the climate crisis. https://oceaniron.org/

Solving the climate-ocean crisis requires both cutting emissions and pursuing carbon dioxide removal (CDR). Past ocean iron fertilization (OIF) experiments in some parts of the ocean have shown that small additions of iron can enhance phytoplankton growth and CO ₂ drawdown. However, prior experiments did not assess the efficacy, durability, or feasibility of OIF for CDR, and broader ecological and biogeochemical responses were not evaluated given the short duration and limited spatial scales. The next generation of OIF field trials must be larger (ca. 1000 km ² ) and longer (>3–6 months) to observe the full response and return to baseline conditions. Potential risks will be assessed, while using community engagement and co-design to create go/no-go decision points. Planning and extrapolating impacts on regional and global scales will require modeling, with the overall goal to provide unbiased assessments and open-source protocols that can guide responsible and rigorous decision-making for any further OIF.

Decarbonization of anthropogenic activities is progressing too slowly, creating an urgent need to actively remove carbon dioxide (CO2) from our atmosphere if we are to prevent the most severe consequences of a disrupted climate system. The marine environment offers several potential approaches for sequestering carbon, with iron-enhanced biological productivity being the most extensively studied. However, past iron addition studies were not primarily aimed at quantifying the durability of carbon storage, nor did they evaluate how prudent this approach might be as a marine carbon dioxide removal (mCDR) approach. A new generation of field studies is needed to address knowledge gaps and uncertainties regarding the effectiveness, scalability, reproducibility, and cost of iron addition for mCDR. These future field experiments need to be conducted on significantly larger spatial scales (over ten times larger) and longer in duration (multi-seasonal rather than the typical one-month studies) compared to previous mesoscale iron addition studies. Core measurements are required to quantify key factors such as: CO2 drawdown in the surface ocean, the re-equilibration timescales of atmospheric CO2 with the surface ocean, the sinking transport of carbon to depth, and the portion of this flux that results in carbon sequestration for 100 years or more. Attention must also be given to the ecological and environmental consequences of iron addition, necessitating a combination of remote sensing, in-situ observations, and modeling. Initial field trials are proposed for the iron-limited high seas of the NE Pacific, chosen for specific reasons outlined in this presentation. These field trials must be developed and conducted in collaboration with social science and governance experts to ensure they are deployed with community engagement, and in an equitable, just, and ethical manner, with the appropriate social safeguards. This presentation reflects the contributions of a diverse group of international and multidisciplinary experts, all of whom are committed to a responsible code of conduct as part of the Exploring Ocean Iron Solutions (ExOIS) consortium. Now is the time for actionable studies to begin. https://oceaniron.org/

Some Rhizosolenia diatoms living in oligotrophic marine ecosystems are known to form large, conspicuous mats and are thought to be sources of new nitrogen to surface waters via vertical migration to the nitracline where subsurface nitrate is accessed for growth. These vertically migrating Rhizosolenia mats are chronically under sampled, and both the diatom species comprising the mats and the associated microbiome have not been characterized using modern molecular techniques. Here we present the first DNA-based analysis of Rhizosolenia mats collected in the North Pacific Subtropical Gyre. Using sequencing of 18S rRNA and nifH genes (a proxy for N2 fixation capacity), we report on the molecular diversity of mat-forming Rhizosolenia species, which include two newly sequenced clades, and an assemblage of associated N2-fixing microorganisms that is distinct from the non-mat associated water column assemblage. Our findings advance knowledge of oligotrophic diatom diversity and challenge prevailing views of their nitrogen sources, suggesting these mats may obtain nitrogen through association-based N2 fixation. Further work is needed to understand the nature of these associations, and whether Rhizosolenia mat communities are a significant unrecognized source of N2-fixation-derived new nitrogen to the oligotrophic surface waters.

Diatoms are major contributors to global primary production and their populations in the modern oceans are affected by availability of iron, nitrogen, phosphate, silica, and other trace metals, vitamins, and infochemicals. However, little is known about the role of phosphorylation in diatoms and its role in regulation and signaling. We report a total of 2759 phosphorylation sites on 1502 proteins detected in Phaeodactylum tricornutum. Conditionally phosphorylated peptides were detected at low iron (n = 108), during the diel cycle (n = 149), and due to nitrogen availability (n = 137). Through a multi-omic comparison of transcript, protein, phosphorylation, and protein homology, we identify numerous proteins and key cellular processes that are likely under control of phospho-regulation. We show that phosphorylation regulates: (1) carbon retrenchment and reallocation during growth under low iron, (2) carbon flux towards lipid biosynthesis after the lights turn on, (3) coordination of transcription and translation over the diel cycle and (4) in response to nitrogen depletion. We also uncover phosphorylation sites for proteins that play major roles in diatom Fe sensing and utilization, including flavodoxin and phytotransferrin (ISIP2A), as well as identify phospho-regulated stress proteins and kinases. These findings provide much needed insight into the roles of protein phosphorylation in diel cycling and nutrient sensing in diatoms.

Diatoms outcompete other phytoplankton for nitrate, yet little is known about the mechanisms underpinning this ability. Genomes and genome-enabled studies have shown that diatoms possess unique features of nitrogen metabolism however, the implications for nutrient utilization and growth are poorly understood. Using a combination of transcriptomics, proteomics, metabolomics, fluxomics, and flux balance analysis to examine short-term shifts in nitrogen utilization in the model pennate diatom in Phaeodactylum tricornutum, we obtained a systems-level understanding of assimilation and intracellular distribution of nitrogen. Chloroplasts and mitochondria are energetically integrated at the critical intersection of carbon and nitrogen metabolism in diatoms. Pathways involved in this integration are organelle-localized GS-GOGAT cycles, aspartate and alanine systems for amino moiety exchange, and a split-organelle arginine biosynthesis pathway that clarifies the role of the diatom urea cycle. This unique configuration allows diatoms to efficiently adjust to changing nitrogen status, conferring an ecological advantage over other phytoplankton taxa.

The phytoplankton community structure of Elkhorn Slough was characterized flow cytometrically and found to be dominated in the upper reaches by small cryptophytes (< 5 microm) and picoeukaryotic phytoplankton (< 3 microm). Cell-specific viability of the small cryptophyte population was quantified along a 5 km transect from the mouth to the shallow upper reaches of Elkhorn Slough using fluorescein diacetate (FDA). Corroborative viability techniques, including SYTOX Green stain and cell digestion assay, were determined to be inappropriate for use in Elkhorn Slough due to indiscriminate staining of suspended particulates and incompatibility with cell target material. Viability analysis with FDA revealed a higher fraction of active cryptophyte cells in the upper reaches, the area of their dominance, and a lower fraction of active cells in the lower slough. It was concluded that cell death (as defined by a lack of FDA-linked esterase enzyme activity) is an important force structuring the phytoplankton community of Elkhorn Slough.

Summary: Photoacclimation consists of short‐ and long‐term strategies used by photosynthetic organisms to adapt to dynamic light environments. Observable photophysiology changes resulting from these strategies have been used in coarse‐grained models to predict light‐dependent growth and photosynthetic rates. However, the contribution of the broader metabolic network, relevant to species‐specific strategies and fitness, is not accounted for in these simple models. We incorporated photophysiology experimental data with genome‐scale modeling to characterize organism‐level, light‐dependent metabolic changes in the model diatomPhaeodactylum tricornutum. Oxygen evolution and photon absorption rates were combined with condition‐specific biomass compositions to predict metabolic pathway usage for cells acclimated to four different light intensities. Photorespiration, an ornithine‐glutamine shunt, and branched‐chain amino acid metabolism were hypothesized as the primary intercompartment reductant shuttles for mediating excess light energy dissipation. Additionally, simulations suggested that carbon shunted through photorespiration is recycled back to the chloroplast as pyruvate, a mechanism distinct from known strategies in photosynthetic organisms. Our results suggest a flexible metabolic network inP. tricornutumthat tunes intercompartment metabolism to optimize energy transport between the organelles, consuming excess energy as needed. Characterization of these intercompartment reductant shuttles broadens our understanding of energy partitioning strategies in this clade of ecologically important primary producers.

Genetic inactivation of diatom nitrate reductase abolishes nitrate assimilation but not nitrate uptake and results in transcriptional activation of nitrate stor

Environmental fluctuations affect distribution, growth and abundance of diatoms in nature, with iron (Fe) availability playing a central role. Studies on the response of diatoms to low Fe have either utilized continuous (24 hr) illumination or sampled a single time of day, missing any temporal dynamics. We profiled the physiology, metabolite composition, and global transcripts of the pennate diatom Phaeodactylum tricornutum during steady-state growth at low, intermediate, and high levels of dissolved Fe over light:dark cycles, to better understand fundamental aspects of genetic control of physiological acclimation to growth under Fe-limitation. We greatly expand the catalog of genes involved in the low Fe response, highlighting the importance of intracellular trafficking in Fe-limited diatoms. P. tricornutum exhibited transcriptomic hallmarks of slowed growth leading to prolonged periods of cell division/silica deposition, which could impact biogeochemical carbon sequestration in Fe-limited regions. Light harvesting and ribosome biogenesis transcripts were generally reduced under low Fe while transcript levels for genes putatively involved in the acquisition and recycling of Fe were increased. We also noted shifts in expression towards increased synthesis and catabolism of branched chain amino acids in P. tricornutum grown at low Fe whereas expression of genes involved in central core metabolism were relatively unaffected, indicating that essential cellular function is protected. Beyond the response of P. tricornutum to low Fe, we observed major coordinated shifts in transcript control of primary and intermediate metabolism over light:dark cycles which contribute to a new view of the significance of distinctive diatom pathways, such as mitochondrial glycolysis and the ornithine-urea cycle. This study provides new insight into transcriptional modulation of diatom physiology and metabolism across light:dark cycles in response to Fe availability, providing mechanistic understanding for the ability of diatoms to remain metabolically poised to respond quickly to Fe input and revealing strategies underlying their ecological success. Oceanic diatoms live in constantly fluctuating environments to which they must adapt in order to survive. During sunlit hours, photosynthesis occurs allowing diatoms to store energy used at night to sustain energy demands. Cellular and molecular mechanisms for regulation of phytoplankton growth are important to understand because of their environmental roles at the base of food webs and in regulating carbon flux out of the atmosphere. In ocean ecosystems, the availability of iron (Fe) commonly limits phytoplankton growth and diatoms typically outcompete other phytoplankton when Fe is added, indicating they have adaptations allowing them to both survive at low Fe and rapidly respond to Fe additions. These adaptations may be unique depending on isolation from coastal or oceanic locations. To identify adaptive strategies, we characterized the response of a model diatom, Phaeodactylum tricornutum, to limiting Fe conditions over day:night cycles using a combination of gene expression analyses, metabolite, and physiology measurements. Major coordinated shifts in metabolism and growth were documented over diel cycles, with peak expression of low Fe expressed genes in the dark phase. Diatoms respond to limiting Fe by increasing Fe acquisition, while decreasing growth rate through slowed cell cycle progression, reduced energy acquisition, and subtle metabolic remodeling.