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Marine diazotrophic cyanobacteria play a crucial role in oceanic nitrogen cycling, supporting primary production and ecosystem balance. Crocosphaera watsonii WH8501 exemplifies this ability by temporally separating photosynthesis and diazotrophy to sustain metabolism. To investigate the regulatory mechanisms underlying this process, we employed LC/MS-MS proteomics in a diel culturing experiment, revealing tightly coordinated protein abundance patterns. Our findings showed a sophisticated temporal regulation of metabolic processes categorized within six distinct protein abundance clusters: (1) nitrogen fixation and amino acid biosynthesis proteins peaked during the night, while (2) glycogen metabolism and dark reactions of photosynthesis were most abundant during the night and day-night transition, likely supporting carbon consumption and energy production. Midday (3 and 4) was dominated by proteins related to photosynthesis, cellular division, and lipid synthesis, whereas late-day peaks (5) in peptide biosynthesis may facilitate nitrogenase complex formation. Notably, the day-night transition (6) exhibited fine-tuned coordination of nitrogenase assembly, with FeS cluster proteins preceding peak nitrogenase iron protein abundance, implying a temporally ordered sequence for functional enzyme formation. Within these categories, sharp temporal patterns emerged in iron trafficking to heme and iron cluster biosynthetic systems, consistent with the need to maintain tight control of iron distribution to metalloproteins at each temporal transition. These results highlight the intricate diel regulation that enables Crocosphaera to balance nitrogen fixation and photosynthesis within a single cell. The observed coordination supports the existence of a complex regulatory system ensuring optimal metabolic performance, reinforcing the critical role of temporal control in sustaining these globally significant biological processes. 

Abstract Recent studies have demonstrated regional differences in marine ecosystem C:N:P with implications for carbon and nutrient cycles. Due to strong co-variance, temperature and nutrient stress explain variability in C:N:P equally well. A reductionistic approach can link changes in individual environmental drivers with changes in biochemical traits and cell C:N:P. Thus, we quantified effects of temperature and nutrient stress on Synechococcus chemistry using laboratory chemostats, chemical analyses, and data-independent acquisition mass spectrometry proteomics. Nutrient supply accounted for most C:N:Pcell variability and induced tradeoffs between nutrient acquisition and ribosomal proteins. High temperature prompted heat-shock, whereas thermal effects via the “translation-compensation hypothesis” were only seen under P-stress. A Nonparametric Bayesian Local Clustering algorithm suggested that changes in lipopolysaccharides, peptidoglycans, and C-rich compatible solutes may also contribute to C:N:P regulation. Physiological responses match field-based trends in ecosystem stoichiometry and suggest a hierarchical environmental regulation of current and future ocean C:N:P. 

Coastal Antarctic marine ecosystems are significant in carbon cycling because of their intense seasonal phytoplankton blooms. Southern Ocean algae are primarily limited by light and iron (Fe) and can be co-limited by cobalamin (vitamin B₁₂). Micronutrient limitation controls productivity and shapes the composition of blooms which are typically dominated by either diatoms or the haptophytePhaeocystis antarctica. However, the vitamin requirements and ecophysiology of the keystone speciesP. antarcticaremain poorly characterized. Using cultures, physiological analysis, and comparative omics, we examined the response ofP. antarcticato a matrix of Fe-B₁₂conditions. We show thatP. antarcticais not auxotrophic for B₁₂, as previously suggested, and identify mechanisms underlying its B₁₂response in cultures of predominantly solitary and colonial cells. A combination of proteomics and proteogenomics reveals a B₁₂-independent methionine synthase fusion protein (MetE-fusion) that is expressed under vitamin limitation and interreplaced with the B₁₂-dependent isoform under replete conditions. Database searches return homologues of the MetE-fusion protein in multiplePhaeocystisspecies and in a wide range of marine microbes, including other photosynthetic eukaryotes with polymorphic life cycles as well as bacterioplankton. Furthermore, we find MetE-fusion homologues expressed in metaproteomic and metatranscriptomic field samples in polar and more geographically widespread regions. As climate change impacts micronutrient availability in the coastal Southern Ocean, our finding thatP. antarcticahas a flexible B₁₂metabolism has implications for its relative fitness compared to B₁₂-auxotrophic diatoms and for the detection of B₁₂-stress in a more diverse set of marine microbes. 

Abstract. Zinc (Zn) is an essential micronutrient for most eukaryotic phytoplankton. Zn uptake by phytoplankton within the euphotic zone results in nutrient-like dissolved Zn (dZn) profiles with a large dynamic range. The combination of key biochemical uses for Zn and large vertical gradients in dZn implies the potential for rapid rates of Zn removal from the surface ocean. However, due to the ease of contamination at sea, direct measurements of dZn uptake within natural environments have not been previously made. To investigate the demand for dZn and for dissolved cadmium (dCd; a closely related nutrient-like element) within Southern Ocean phytoplankton communities, we conducted 67Zn and 110Cd tracer uptake experiments within the Amundsen Sea, Ross Sea, and Terra Nova Bay of the Southern Ocean. We observed a high magnitude of Zn uptake (ρZn > 100 pmol dZn L−1 d−1) into the particulate phase that was consistent with ambient depleted dZn surface concentrations. High biomass and low partial pressure of carbon dioxide in seawater (seawater pCO2) appeared to contribute to ρZn, which also led to increases in ρCd likely through the upregulation of shared transport systems. These high ρZn measurements further imply that only short timescales are needed to deplete the large winter dZn inventory down to the observed surface levels in this important carbon-capturing region. Overall, the high magnitude of Zn uptake into the particulate fraction suggests that even in the Zn-rich waters of the Southern Ocean, high Zn uptake rates can lead to Zn depletion and potential Zn scarcity. 

Abstract Many marine microbes require vitamin B12 (cobalamin) but are unable to synthesize it, necessitating reliance on other B12-producing microbes. Thus, phytoplankton and bacterioplankton community dynamics can partially depend on the production and release of a limiting resource by members of the same community. We tested the impact of temperature and B12 availability on the growth of two bacterial taxa commonly associated with phytoplankton: Ruegeria pomeroyi, which produces B12 and fulfills the B12 requirements of some phytoplankton, and Alteromonas macleodii, which does not produce B12 but also does not strictly require it for growth. For B12-producing R. pomeroyi, we further tested how temperature influences B12 production and release. Access to B12 significantly increased growth rates of both species at the highest temperatures tested (38 °C for R. pomeroyi, 40 °C for A. macleodii) and A. macleodii biomass was significantly reduced when grown at high temperatures without B12, indicating that B12 is protective at high temperatures. Moreover, R. pomeroyi produced more B12 at warmer temperatures but did not release detectable amounts of B12 at any temperature tested. Results imply that increasing temperatures and more frequent marine heatwaves with climate change will influence microbial B12 dynamics and could interrupt symbiotic resource sharing. 

Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO 2 , NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.