Marine Synechococcus are some of the most diverse and ubiquitous phytoplankton, and iron (Fe) is an essential micronutrient that limits productivity in many parts of the ocean. To investigate how ...coastal and oceanic Atlantic Synechococcus strains acclimate to Fe availability, we compared the growth, photophysiology, and quantitative proteomics of two Synechococcus strains from different Fe regimes. Synechococcus strain WH8102, from a region in the southern Sargasso Sea that receives substantial dust deposition, showed impaired growth and photophysiology as Fe declined, yet used few acclimation responses. Coastal WH8020, from the dynamic, seasonally variable New England shelf, displayed a multitiered, hierarchical cascade of acclimation responses with different Fe thresholds. The multitiered response included changes in Fe acquisition, storage, and photosynthetic proteins, substitution of flavodoxin for ferredoxin, and modified photophysiology, all while maintaining remarkably stable growth rates over a range of Fe concentrations. Modulation of two distinct ferric uptake regulator (Fur) proteins that coincided with the multitiered proteome response was found, implying the coastal strain has different regulatory threshold responses to low Fe availability. Low nitrogen (N) and phosphorus (P) availability in the open ocean may favor the loss of Fe response genes when Fe availability is consistent over time, whereas these genes are retained in dynamic environments where Fe availability fluctuates and N and P are more abundant.
Dissolved organic phosphorus (DOP) concentration distributions in the global surface ocean inform our understanding of marine biogeochemical processes such as nitrogen fixation and primary ...production. The spatial distribution of DOP concentrations in the surface ocean reflect production by primary producers and consumption as an organic nutrient by phytoplankton including diazotrophs and other microbes, as well as other loss processes such as photolysis. Compared to dissolved organic carbon and nitrogen, however, relatively few marine DOP concentration measurements have been made, largely due to the lack of automated analysis techniques. Here we present a database of marine DOP concentration measurements (DOPv2021) that includes new (n = 730) and previously published (n = 3140) observations made over the last ~30 years (1990-2021), including 1751 observations in the upper 50 m. This dataset encompasses observations from all major ocean basins including the poorly represented Indian, South Pacific, and Southern Oceans and provides insight into spatial distributions of DOP in the ocean. It is also valuable for researchers who work on marine primary production and nitrogen fixation.
Reactive oxygen species (ROS) like superoxide drive rapid transformations of carbon and metals in aquatic systems and play dynamic roles in biological health, signaling, and defense across a ...diversity of cell types. In phytoplankton, however, the ecophysiological role(s) of extracellular superoxide production has remained elusive. Here, the mechanism and function of extracellular superoxide production by the marine diatom Thalassiosira oceanica are described. Extracellular superoxide production in T. oceanica exudates was coupled to the oxidation of NADPH. A putative NADPH-oxidizing flavoenzyme with predicted transmembrane domains and high sequence similarity to glutathione reductase (GR) was implicated in this process. GR was also linked to extracellular superoxide production by whole cells via quenching by the flavoenzyme inhibitor diphenylene iodonium (DPI) and oxidized glutathione, the preferred electron acceptor of GR. Extracellular superoxide production followed a typical photosynthesis-irradiance curve and increased by 30% above the saturation irradiance of photosynthesis, while DPI significantly impaired the efficiency of photosystem II under a wide range of light levels. Together, these results suggest that extracellular superoxide production is a byproduct of a transplasma membrane electron transport system that serves to balance the cellular redox state through the recycling of photosynthetic NADPH. This photoprotective function may be widespread, consistent with the presence of putative homologs to T. oceanica GR in other representative marine phytoplankton and ocean metagenomes. Given predicted climate-driven shifts in global surface ocean light regimes and phytoplankton community-level photoacclimation, these results provide implications for future ocean redox balance, ecological functioning, and coupled biogeochemical transformations of carbon and metals.
Diatoms are responsible for ∼40% of marine primary production and are key players in global carbon cycling. There is mounting evidence that diatom growth is influenced by cobalamin (vitamin B 12 ) ...availability. This cobalt-containing micronutrient is only produced by some bacteria and archaea but is required by many diatoms and other eukaryotic phytoplankton. Despite its potential importance, little is known about mechanisms of cobalamin acquisition in diatoms or the impact of cobalamin scarcity on diatom molecular physiology. Proteomic profiling and RNA-sequencing transcriptomic analysis of the cultured diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana revealed three distinct strategies used by diatoms to cope with low cobalamin: increased cobalamin acquisition machinery, decreased cobalamin demand, and management of reduced methionine synthase activity through changes in folate and S-adenosyl methionine metabolism. One previously uncharacterized protein, cobalamin acquisition protein 1 (CBA1), was up to 160-fold more abundant under low cobalamin availability in both diatoms. Autologous overexpression of CBA1 revealed association with the outside of the cell and likely endoplasmic reticulum localization. Cobalamin uptake rates were elevated in strains overexpressing CBA1, directly linking this protein to cobalamin acquisition. CBA1 is unlike characterized cobalamin acquisition proteins and is the only currently identified algal protein known to be implicated in cobalamin uptake. The abundance and widespread distribution of transcripts encoding CBA1 in environmental samples suggests that cobalamin is an important nutritional factor for phytoplankton. Future study of CBA1 and other molecular signatures of cobalamin scarcity identified here will yield insight into the evolution of cobalamin utilization and facilitate monitoring of cobalamin starvation in oceanic diatom communities.
Prochlorococcus contributes significantly to ocean primary productivity. The link between primary productivity and iron in specific ocean regions is well established and iron limitation of ...Prochlorococcus cell division rates in these regions has been shown. However, the extent of ecotypic variation in iron metabolism among Prochlorococcus and the molecular basis for differences is not understood. Here, we examine the growth and transcriptional response of Prochlorococcus strains, MED4 and MIT9313, to changing iron concentrations. During steady state, MIT9313 sustains growth at an order-of-magnitude lower iron concentration than MED4. To explore this difference, we measured the whole-genome transcriptional response of each strain to abrupt iron starvation and rescue. Only four of the 1159 orthologs of MED4 and MIT9313 were differentially expressed in response to iron in both strains. However, in each strain, the expression of over a hundred additional genes changed, many of which are in labile genomic regions, suggesting a role for lateral gene transfer in establishing diversity of iron metabolism among Prochlorococcus. Furthermore, we found that MED4 lacks three genes near the iron-deficiency-induced gene (idiA) that are present and induced by iron stress in MIT9313. These genes are interesting targets for studying the adaptation of natural Prochlorococcus assemblages to local iron conditions as they show more diversity than other genomic regions in environmental metagenomic databases.
Shotgun mass spectrometry was used to detect proteins in the harmful alga, Aureococcus anophagefferens, and monitor their relative abundance across nutrient replete (control), phosphate-deficient ...(-P) and -P refed with phosphate (P-refed) conditions. Spectral counting techniques identified differentially abundant proteins and demonstrated that under phosphate deficiency, A. anophagefferens increases proteins involved in both inorganic and organic phosphorus (P) scavenging, including a phosphate transporter, 5'-nucleotidase, and alkaline phosphatase. Additionally, an increase in abundance of a sulfolipid biosynthesis protein was detected in -P and P-refed conditions. Analysis of the polar membrane lipids showed that cellular concentrations of the sulfolipid sulphoquinovosyldiacylglycerol (SQDG) were nearly two-fold greater in the -P condition versus the control condition, while cellular phospholipids were approximately 8-fold less. Transcript and protein abundances were more tightly coupled for gene products involved in P metabolism compared to those involved in a range of other metabolic functions. Comparison of protein abundances between the -P and P-refed conditions identified differences in the timing of protein degradation and turnover. This suggests that culture studies examining nutrient starvation responses will be valuable in interpreting protein abundance patterns for cellular nutritional status and history in metaproteomic datasets.
Adenylylsulfate reductase (Apr) is a flavoprotein with a dissimilatory sulfate reductase function. Its ability to catalyze the reverse reaction in sulfur oxidizers has propelled a complex ...phylogenetic history of transfers with sulfate reducers and made this enzyme an important protein in ocean sulfur cycling. As part of a graduate course, we analyzed metaproteomic data from the Ocean Protein Portal and observed evidence of Apr alpha (AprA) and beta (AprB) subunits in the Central Pacific Ocean. The protein was originally taxonomically attributed toChlorobium tepidum TLS, a green sulfur bacterium. However, our phylogenomic and oceanographic contextual analysis contradicted this label, instead showing that this protein is consistent with the genomic material from the newly discovered Candidatus Lambdaproteobacteriaclass, implying that the ecological role of this lineage in oxygen minimum twilight zones is underappreciated. This study illustrates how metaproteogenomic analysis can contribute to more accurate metagenomic/proteomic annotations and comprehensive ocean biogeochemical processes conducive to course-based research experiences.
Summary
Diatoms are a highly successful group of photosynthetic protists that often thrive under adverse environmental conditions. Members of the genus Pseudo‐nitzschia are ecologically important ...diatoms which are able to subsist during periods of chronic iron limitation and form dense blooms following iron fertilization events. The cellular strategies within diatoms that orchestrate these physiological responses to variable iron concentrations remain largely uncharacterized. Using a combined transcriptomic and proteomic approach, we explore the exceptional ability of a diatom isolated from the iron‐limited Northeast Pacific Ocean to reorganize its intracellular processes as a function of iron. We compared the molecular responses of Pseudo‐nitzschia granii observed under iron‐replete and iron‐limited growth conditions to those of other model diatoms. Iron‐coordinated molecular responses demonstrated some agreement between gene expression and protein abundance, including iron‐starvation‐induced‐proteins, a putative iron transport system and components of photosynthesis and the Calvin cycle. Pseudo‐nitzschia granii distinctly differentially expresses genes encoding proteins involved in iron‐independent photosynthetic electron transport, urea acquisition and vitamin synthesis. We show that P. granii is unique among studied diatoms in its physiology stemming from distinct cellular responses, which may underlie its ability to subsist in low iron regions and rapidly bloom to outcompete other diatom taxa following iron enrichment.
We have measured the isotopic fractionation of zinc (Zn) during uptake by the marine diatom Thalassiosira oceanica cultured at a range of free Zn2+ concentrations representative of the natural range ...from coastal and oligotrophic regions of the ocean. Harvested cells were rinsed with either plain seawater or a wash designed to remove adsorbed extracellular metals. Unwashed cells had much higher levels of Zn and were isotopically heavier than the media, indicating a positive isotope effect for extracellular Zn adsorption. Internalized Zn, measured in washed cells, was isotopically lighter than the media. The magnitude of Zn isotope fractionation changed with free Zn2+ concentration, corresponding to a switch on the part of T. oceanica between the predominance of high- and low-affinity Zn transport pathways. The total isotope effect for uptake ($Delta^{66}Zn$) was $-0.2 \textperthousand$ for high-affinity uptake at low Zn concentrations and $-0.8\textperthousand$ at the highest Zn concentrations, where low-affinity uptake is dominant. To our knowledge, this is the first study to describe a physiological basis for biological metal isotope fractionation during transport across the cell membrane. Similar high- and low-affinity Zn transport pathways are common among marine phytoplankton, suggesting that the processes described here are an important factor in natural marine Zn isotope variations.
We present full-depth zonal sections of total dissolved cobalt, iron, manganese, and labile cobalt from the South Atlantic Ocean. A basin-scale plume from the African coast appeared to be a major ...source of dissolved metals to this region, with high cobalt concentrations in the oxygen minimum zone of the Angola Dome and extending 2500 km into the subtropical gyre. Metal concentrations were elevated along the coastal shelf, likely due to reductive dissolution and resuspension of particulate matter. Linear relationships between cobalt, N₂O, and O₂, as well as low surface aluminum supported a coastal rather than atmospheric cobalt source. Lateral advection coupled with upwelling, biological uptake, and remineralization delivered these metals to the basin, as evident in two zonal transects with distinct physical processes that exhibited different metal distributions. Scavenging rates within the coastal plume differed for the three metals; iron was removed fastest, manganese removal was 2.5 times slower, and cobalt scavenging could not be discerned from water mass mixing. Because scavenging, biological utilization, and export constantly deplete the oceanic inventories of these three hybrid-type metals, point sources of the scale observed here likely serve as vital drivers of their oceanic cycles. Manganese concentrations were elevated in surface waters across the basin, likely due to coupled redox processes acting to concentrate the dissolved species there. These observations of basin-scale hybrid metal plumes combined with the recent projections of expanding oxygen minimum zones suggest a potential mechanism for effects on ocean primary production and nitrogen fixation via increases in trace metal source inputs.
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