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ABSTRACT The continental shelf of the Western Antarctic Peninsula (WAP) is a highly variable system characterized by strong cross-shelf gradients, rapid regional change, and large blooms of phytoplankton, notably diatoms. Rapid environmental changes coincide with shifts in plankton community composition and productivity, food web dynamics, and biogeochemistry. Despite the progress in identifying important environmental factors influencing plankton community composition in the WAP, the molecular basis for their survival in this oceanic region, as well as variations in species abundance, metabolism, and distribution, remains largely unresolved. Across a gradient of physicochemical parameters, we analyzed the metabolic profiles of phytoplankton as assessed through metatranscriptomic sequencing. Distinct phytoplankton communities and metabolisms closely mirrored the strong gradients in oceanographic parameters that existed from coastal to offshore regions. Diatoms were abundant in coastal, southern regions, where colder and fresher waters were conducive to a bloom of the centric diatom,Actinocyclus. Members of this genus invested heavily in growth and energy production; carbohydrate, amino acid, and nucleotide biosynthesis pathways; and coping with oxidative stress, resulting in uniquely expressed metabolic profiles compared to other diatoms. We observed strong molecular evidence for iron limitation in shelf and slope regions of the WAP, where diatoms in these regions employed iron-starvation induced proteins, a geranylgeranyl reductase, aquaporins, and urease, among other strategies, while limiting the use of iron-containing proteins. The metatranscriptomic survey performed here reveals functional differences in diatom communities and provides further insight into the environmental factors influencing the growth of diatoms and their predicted response to changes in ocean conditions. IMPORTANCEIn the Southern Ocean, phytoplankton must cope with harsh environmental conditions such as low light and growth-limiting concentrations of the micronutrient iron. Using metratranscriptomics, we assessed the influence of oceanographic variables on the diversity of the phytoplankton community composition and on the metabolic strategies of diatoms along the Western Antarctic Peninsula, a region undergoing rapid climate change. We found that cross-shelf differences in oceanographic parameters such as temperature and variable nutrient concentrations account for most of the differences in phytoplankton community composition and metabolism. We opportunistically characterized the metabolic underpinnings of a large bloom of the centric diatomActinocyclusin coastal waters of the WAP. Our results indicate that physicochemical differences from onshore to offshore are stronger than between southern and northern regions of the WAP; however, these trends could change in the future, resulting in poleward shifts in functional differences in diatom communities and phytoplankton blooms. 

Protist plankton can be divided into three main groups: phytoplankton, zooplankton, and mixoplankton.In situmethods for studying phytoplankton and zooplankton are relatively straightforward since they generally target chlorophyll/photosynthesis or grazing activity, while the integration of both processes within a single cell makes mixoplankton inherently challenging to study. As a result, we understand less about mixoplankton physiology and their role in food webs, biogeochemical cycling, and ecosystems compared to phytoplankton and zooplankton. In this paper, we posit that by merging conventional techniques, such as microscopy and physiological data, with innovative methods likein situsingle-cell sorting and omics datasets, in conjunction with a diverse array of modeling approaches ranging from single-cell modeling to comprehensive Earth system models, we can propel mixoplankton research into the forefront of aquatic ecology. We present eight crucial research questions pertaining to mixoplankton and mixotrophy, and briefly outline a combination of existing methods and models that can be used to address each question. Our intent is to encourage more interdisciplinary research on mixoplankton, thereby expanding the scope of data acquisition and knowledge accumulation for this understudied yet critical component of aquatic ecosystems. 

Microeukaryotes (protists) serve fundamental roles in the marine environment as contributors to biogeochemical nutrient cycling and ecosystem function. Their activities can be inferred through metatranscriptomic investigations, which provide a detailed view into cellular processes, chemical-biological interactions in the environment, and ecological relationships among taxonomic groups. Established workflows have been individually put forth describing biomass collection at sea, laboratory RNA extraction protocols, and bioinformatic processing and computational approaches. Here, we present a compilation of current practices and lessons learned in carrying out metatranscriptomics of marine pelagic protistan communities, highlighting effective strategies and tools used by practitioners over the past decade. We anticipate that these guidelines will serve as a roadmap for new marine scientists beginning in the realms of molecular biology and/or bioinformatics, and will equip readers with foundational principles needed to delve into protistan metatranscriptomics. 

Abstract Phago-mixotrophy, the combination of photoautotrophy and phagotrophy in mixoplankton, organisms that can combine both trophic strategies, have gained increasing attention over the past decade. It is now recognized that a substantial number of protistan plankton species engage in phago-mixotrophy to obtain nutrients for growth and reproduction under a range of environmental conditions. Unfortunately, our current understanding of mixoplankton in aquatic systems significantly lags behind our understanding of zooplankton and phytoplankton, limiting our ability to fully comprehend the role of mixoplankton (and phago-mixotrophy) in the plankton food web and biogeochemical cycling. Here, we put forward five research directions that we believe will lead to major advancement in the field: (i) evolution: understanding mixotrophy in the context of the evolutionary transition from phagotrophy to photoautotrophy; (ii) traits and trade-offs: identifying the key traits and trade-offs constraining mixotrophic metabolisms; (iii) biogeography: large-scale patterns of mixoplankton distribution; (iv) biogeochemistry and trophic transfer: understanding mixoplankton as conduits of nutrients and energy; and (v) in situ methods: improving the identification of in situ mixoplankton and their phago-mixotrophic activity. 

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 ZCRPs 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. 

Abstract The keystone marine nitrogen fixer Trichodesmium thrives in high-dust environments. While laboratory investigations have observed that Trichodesmium colonies can access the essential nutrient iron from dust particles, less clear are the biochemical strategies underlying particle–colony interactions in nature. Here we demonstrate that Trichodesmium colonies engage with mineral particles in the wild with distinct molecular responses. We encountered particle-laden Trichodesmium colonies 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, 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 that Trichodesmium was 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 to Trichodesmium’s ecological success and global biogeochemical impact, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling. 

Abstract. Bioactive trace metals are critical micronutrients for marinemicroorganisms due to their role in mediating biological redox reactions,and complex biogeochemical processes control their distributions.Hydrothermal vents may represent an important source of metals tomicroorganisms, especially those inhabiting low-iron waters, such as in thesouthwest Pacific Ocean. Previous measurements of primordial 3Heindicate a significant hydrothermal source originating in the northeastern (NE)Lau Basin, with the plume advecting into the southwest Pacific Ocean at1500–2000 m depth (Lupton etal., 2004). Studies investigating the long-range transport of trace metalsassociated with such dispersing plumes are rare, and the biogeochemicalimpacts on local microbial physiology have not yet been described. Here wequantified dissolved metals and assessed microbial metaproteomes across atransect spanning the tropical and equatorial Pacific with a focus on thehydrothermally active NE Lau Basin and report elevated iron and manganeseconcentrations across 441 km of the southwest Pacific. The most intensesignal was detected near the Mangatolo Triple Junction (MTJ) and NortheastLau Spreading Center (NELSC), in close proximity to the previously reported3He signature. Protein content in distal-plume-influenced seawater,which was high in metals, was overall similar to background locations,though key prokaryotic proteins involved in metal and organic uptake,protein degradation, and chemoautotrophy were abundant compared to deepwaters outside of the distal plume. Our results demonstrate that tracemetals derived from the NE Lau Basin are transported over appreciabledistances into the southwest Pacific Ocean and that bioactive chemicalresources released from submarine vent systems are utilized by surroundingdeep-sea microbes, influencing both their physiology and their contributionsto ocean biogeochemical cycling. 

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 transcriptome 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.