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Abstract Scarce dissolved surface ocean concentrations of the essential algal micronutrient zinc suggest that Zn may influence the growth of phytoplankton such as diatoms, which are major contributors to marine primary productivity. However, the specific mechanisms by which diatoms acclimate to Zn deficiency are poorly understood. Using global proteomic analysis, we identified two proteins (ZCRP-A/B, Zn/Co Responsive Protein A/B) among four diatom species that became abundant under Zn/Co limitation. Characterization using reverse genetic techniques and homology data suggests putative Zn/Co chaperone and membrane-bound transport complex component roles for ZCRP-A (a COG0523 domain protein) and ZCRP-B, respectively. Metaproteomic detection of ZCRPsmore »along a Pacific Ocean transect revealed increased abundances at the surface (<200 m) where dZn and dCo were scarcest, implying Zn nutritional stress in marine algae is more prevalent than previously recognized. These results demonstrate multiple adaptive responses to Zn scarcity in marine diatoms that are deployed in low Zn regions of the Pacific Ocean.« less

Abstract Pseudoalteromonas (BB2-AT2) is a ubiquitous marine heterotroph, often associated with labile organic carbon sources in the ocean (e.g. phytoplankton blooms and sinking particles). Heterotrophs hydrolyze exported photosynthetic materials, components of the biological carbon pump, with the use of diverse metalloenzymes containing zinc (Zn), manganese (Mn), cobalt (Co), and nickel (Ni). Studies on the metal requirements and cytosolic utilization of metals for marine heterotrophs are scarce, despite their relevance to global carbon cycling. Here, we characterized the Zn, Mn, Co, and Ni metallome of BB2-AT2. We found that the Zn metallome is complex and cytosolic Zn is associated with numerousmore »proteins for transcription (47.2% of the metallome, obtained from singular value decomposition of the metalloproteomic data), translation (33.5%), proteolysis (12.8%), and alkaline phosphatase activity (6.4%). Numerous proteolytic enzymes also appear to be putatively associated with Mn, and to a lesser extent, Co. Putative identification of the Ni-associated proteins, phosphoglucomutase and a protein in the cupin superfamily, provides new insights for Ni utilization in marine heterotrophs. BB2-AT2 relies on numerous transition metals for proteolytic and phosphatase activities, inferring an adaptative potential to metal limitation. Our field observations of increased alkaline phosphatase activity upon addition of Zn in field incubations suggest that such metal limitation operates in sinking particulate material collected from sediment traps. Taken together, this study improves our understanding of the Zn, Mn, Co, and Ni metallome of marine heterotrophic bacteria and provides novel and mechanistic frameworks for understanding the influence of nutrient limitation on biogeochemical cycling.« less

The keystone marine nitrogen fixerTrichodesmiumthrives in high-dust environments. While laboratory investigations have observed thatTrichodesmiumcolonies can access the essential nutrient iron from dust particles, less clear are the biochemical strategies underlying particle–colony interactions in nature. Here we demonstrate thatTrichodesmiumcolonies engage with mineral particles in the wild with distinct molecular responses. We encountered particle-ladenTrichodesmiumcolonies at a sampling location in the Southern Caribbean Sea; microscopy and synchrotron-based imaging then demonstrated heterogeneous associations with iron oxide and iron-silicate minerals. Metaproteomic analysis of individual colonies by a new low-biomass approach revealed responses in biogeochemically relevant proteins including photosynthesis proteins and metalloproteins containing iron, nickel, copper,more »and zinc. The iron-storage protein ferritin was particularly enriched implying accumulation of mineral-derived iron, and multiple iron acquisition pathways including Fe(II), Fe(III), and Fe-siderophore transporters were engaged. While the particles provided key trace metals such as iron and nickel, there was also evidence thatTrichodesmiumwas altering its strategy to confront increased superoxide production and metal exposure. Chemotaxis regulators also responded to mineral presence suggesting involvement in particle entrainment. These molecular responses are fundamental toTrichodesmium’secological success and global biogeochemical impact, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling.

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Fe is a critical nutrient to the marine biological pump, which is the process that exports photosynthetically fixed carbon in the upper ocean to the deep ocean. Fe limitation controls photosynthetic activity in major regions of the oceans, and the subsequent degradation of exported photosynthetic material is facilitated particularly by marine heterotrophic bacteria. Despite their importance in the carbon cycle and the scarcity of Fe in seawater, the Fe requirements, storage and cytosolic utilization of these marine heterotrophs has been less studied. Here, we characterized the Fe metallome of Pseudoalteromonas (BB2-AT2). We found that with two copies of bacterioferritin (Bfr),more »Pseudoalteromonas possesses substantial capacity for luxury uptake of Fe. Fe : C in the whole cell metallome was estimated (assuming C : P stoichiometry ∼51 : 1) to be between ∼83 μmol : mol Fe : C, ∼11 fold higher than prior marine bacteria surveys. Under these replete conditions, other major cytosolic Fe-associated proteins were observed including superoxide dismutase (SodA; with other metal SOD isoforms absent under Fe replete conditions) and catalase (KatG) involved in reactive oxygen stress mitigation and aconitase (AcnB), succinate dehydrogenase (FrdB) and cytochromes (QcrA and Cyt1) involved in respiration. With the aid of singular value decomposition (SVD), we were able to computationally attribute peaks within the metallome to specific metalloprotein contributors. A putative Fe complex TonB transporter associated with the closely related Alteromonas bacterium was found to be abundant within the Pacific Ocean mesopelagic environment. Despite the extreme scarcity of Fe in seawater, the marine heterotroph Pseudoalteromonas has expansive Fe storage capacity and utilization strategies, implying that within detritus and sinking particles environments, there is significant opportunity for Fe acquisition. Together these results imply an evolved dedication of marine Pseudoalteromonas to maintaining an Fe metalloproteome, likely due to its dependence on Fe-based respiratory metabolism.« less

Marine microeukaryotes play a fundamental role in biogeochemical cycling through the transfer of energy to higher trophic levels and vertical carbon transport. Despite their global importance, microeukaryote physiology, nutrient metabolism and contributions to carbon cycling across offshore ecosystems are poorly characterized. Here, we observed the prevalence of dinoflagellates along a 4,600-km meridional transect extending across the central Pacific Ocean, where oligotrophic gyres meet equatorial upwelling waters rich in macronutrients yet low in dissolved iron. A combined multi-omics and geochemical analysis provided a window into dinoflagellate metabolism across the transect, indicating a continuous taxonomic dinoflagellate community that shifted its functional transcriptomemore »and proteome as it extended from the euphotic to the mesopelagic zone. In euphotic waters, multi-omics data suggested that a combination of trophic modes were utilized, while mesopelagic metabolism was marked by cytoskeletal investments and nutrient recycling. Rearrangement in nutrient metabolism was evident in response to variable nitrogen and iron regimes across the gradient, with no associated change in community assemblage. Total dinoflagellate proteins scaled with particulate carbon export, with both elevated in equatorial waters, suggesting a link between dinoflagellate abundance and total carbon flux. Dinoflagellates employ numerous metabolic strategies that enable broad occupation of central Pacific ecosystems and play a dual role in carbon transformation through both photosynthetic fixation in the euphotic zone and remineralization in the mesopelagic zone.« less