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The oceans contain large reservoirs of inorganic and organic carbon and play a critical role in both global carbon cycling and climate. Most of the biogeochemical transformations in the oceans are driven by marine microbes. Thus, molecular processes occurring at the scale of single cells govern global geochemical dynamics, posing a challenge of scales. Understanding the processes controlling ocean carbon cycling from the cellular to the global scale requires the integration of multiple disciplines including microbiology, ecology, biogeochemistry, and computational fields such as numerical models and bioinformatics. A shared language and foundational knowledge will facilitate these interactions. This review provides the state of knowledge on the role marine microbes play in large-scale ocean carbon cycling through the lens of observational oceanography and biogeochemical models. We conclude by outlining ways in which the field can bridge the gap between -omics datasets and ocean models to understand ocean carbon cycling across scales. 

Mixotrophic protists combine photosynthesis with the ingestion of prey to thrive in resource-limited conditions in the ocean. Yet, how they fine-tune resource investments between their two different metabolic strategies remains unclear. Here, we present a modeling framework (Mixotroph Optimal Contributions to Heterotrophy and Autotrophy) that predicts the optimal (growth-maximizing) investments of carbon and nitrogen as a function of environmental conditions. Our model captures a full spectrum of trophic modes, in which the optimal investments reflect zero-waste solutions (i.e., growth is colimited by carbon and nitrogen) and accurately reproduces experimental results. By fitting the model to data forOchromonas, we were able to predict metabolic strategies at a global scale. We find that high phagotrophic investment is the dominant strategy across different oceanic biomes, used primarily for nitrogen acquisition. Our results therefore support empirical observations of the importance of mixotrophic grazers to upper ocean bacterivory. 

Phytoplankton are responsible for half of all oxygen production and drive the ocean carbon cycle. Metabolic theory predicts that increasing global temperatures will cause phytoplankton to become more heterotrophic and smaller. Here, we uncover the metabolic trade-offs between cellular space, energy, and stress management driving phytoplankton thermal acclimation and how these might be overcome through evolutionary adaptation. We show that the observed relationships between traits such as chlorophyll, lipid content, C:N, and size can be predicted on the basis of the metabolic demands of the cell, the thermal dependency of transporters, and changes in membrane lipids. We suggest that many of the observed relationships are not fixed physiological constraints but rather can be altered through adaptation. For example, the evolution of lipid metabolism can favor larger cells with higher lipid content to mitigate oxidative stress. These results have implications for rates of carbon sequestration and export in a warmer ocean. 

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. 

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.