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Abstract The daily cycle of solar radiation has a profound influence in structuring the physiology of microbes in the euphotic zone and subsequently setting the degree of coupling across trophic levels within ocean ecosystems. There has been an upsurge of interest in the biological role of the diel cycle and the ability to probe it using molecular approaches (i.e., “omics”), which now allow us to pinpoint the level of detail of the diel cycle that is required to better understand microbes' roles across multiple biogeochemical cycles. Although sampling the diel cycle requires additional resources, the payback is large. A better understanding of the diel cycle provides a holistic framework with which to align patterns and causal sequences across multi‐omic layers, yielding consequent connections with metabolic processes to develop more robust mechanistic models. Such models provide the stepping stones to better understand how resource allocation in cells is driven by environmental forcing.more » « less
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Abstract Coccolithophores fix organic carbon and produce calcite plates (coccoliths) that ballast organic matter and facilitate carbon export. Photosynthesis consumes carbon dioxide, while calcification produces it, raising questions about whether coccolithophores are a net sink or source of carbon. We characterized the physiology of calcified and noncalcified (“naked”) phenotypes ofEmiliania huxleyi(CCMP374) and investigated the relationship between calcification and photosynthesis across a gradient of light (25–2000 μmol photons m−2 s−1) spanning the euphotic zone. Growth and photophysiological parameters increased with light until reaching a mid‐light (150 μmol photons m−2 s−1) maximum for both phenotypes. Calcified cells were characterized by enhanced photophysiology and less photoinhibition. Further, enhanced bicarbonate transport in calcified cells led to higher rates of particulate organic carbon fixation and growth compared to naked cells at mid‐light to high light (150–2000 μmol photons m−2 s−1). Coccolith production was similarly high at mid and high light, but the rate of coccolith shedding was >3‐fold lower at high‐light (1.2 vs. 0.35 coccoliths cell−1 h−1). The cellular mechanims(s) of this differential shedding remain unknown and underly light‐related controls on coccosphere maintenance. Our data suggest coccoliths shade cells at high light and that enhanced bicarbonate transport associated with calcification increases internal carbon supplies available for organic carbon fixation.more » « less
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Abstract The cycling of marine particulate matter is critical for sequestering carbon in the deep ocean and in marine sediments. Biogenic minerals such as calcium carbonate (CaCO3) and opal add density to more buoyant organic material, facilitating particle sinking and export. Here, we compile and analyze a global data set of particulate organic carbon (POC), particulate inorganic carbon (PIC, or CaCO3), and biogenic silica (bSi, or opal) concentrations collected using large volume pumps (LVPs). We analyze the distribution of all three biogenic phases in the small (1–53 μm) and large (>53 μm) size classes. Over the entire water column 76% of POC exists in the small size fraction. Similarly, the small size class contains 82% of PIC, indicating the importance of small‐sized coccolithophores to the PIC budget of the ocean. In contrast, 50% of bSi exists in the large size fraction, reflecting the larger size of diatoms and radiolarians compared with coccolithophores. We use PIC:POC and bSi:POC ratios in the upper ocean to document a consistent signal of shallow mineral dissolution, likely linked to biologically mediated processes. Sediment trap PIC:POC and bSi:POC are elevated with respect to LVP samples and increase strongly with depth, indicating the concentration of mineral phases and/or a deficit of POC in large sinking particles. We suggest that future sampling campaigns pair LVPs with sediment traps to capture the full particulate field, especially the large aggregates that contribute to mineral‐rich deep ocean fluxes, and may be missed by LVPs.more » « less
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Identifying mechanisms driving the substantial dissolution of biogenic CaCO3(60 to 80%) in surface and mesopelagic waters of the global ocean is critical for constraining the surface ocean’s alkalinity and inorganic carbon budgets. We examine microzooplankton grazing on coccolithophores, photosynthetic calcifying algae responsible for a majority of open-ocean CaCO3production, as a mechanism driving shallow dissolution. We show that microzooplankton grazing dissolves 92 ± 7% of ingested coccolith calcite, which may explain 50 to 100% of the observed CaCO3dissolution in supersaturated surface waters. Microzooplankton grazing on coccolithophores is thus a substantial, previously unrecognized biological mechanism affecting the ballasting of organic carbon to deeper waters, the ecology and fitness of microzooplankton themselves due to buffering of food vacuole pH, and ultimately the continued ability of the surface ocean to take up atmospheric carbon dioxide.more » « less
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Gravity-driven sinking of “marine snow” sequesters carbon in the ocean, constituting a key biological pump that regulates Earth’s climate. A mechanistic understanding of this phenomenon is obscured by the biological richness of these aggregates and a lack of direct observation of their sedimentation physics. Utilizing a scale-free vertical tracking microscopy in a field setting, we present microhydrodynamic measurements of freshly collected marine snow aggregates from sediment traps. Our observations reveal hitherto-unknown comet-like morphology arising from fluid-structure interactions of transparent exopolymer halos around sinking aggregates. These invisible comet tails slow down individual particles, greatly increasing their residence time. Based on these findings, we constructed a reduced-order model for the Stokesian sedimentation of these mucus-embedded two-phase particles, paving the way toward a predictive understanding of marine snow.more » « less
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Lipids comprise a significant fraction of sinking organic matter in the ocean and play a crucial role in the carbon cycle. Despite this, our understanding of the processes that control lipid degradation is limited. We combined nanolipidomics and imaging to study the bacterial degradation of diverse algal lipid droplets and found that bacteria isolated from marine particles exhibited distinct dietary preferences, ranging from selective to promiscuous degraders. Dietary preference was associated with a distinct set of lipid degradation genes rather than with taxonomic origin. Using synthetic communities composed of isolates with distinct dietary preferences, we showed that lipid degradation is modulated by microbial interactions. A particle export model incorporating these dynamics indicates that metabolic specialization and community dynamics may influence lipid transport efficiency in the ocean’s mesopelagic zone.more » « less
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Lauritano, Chiara; Ianora, Adrianna (Ed.)Ecophysiological stress and the grazing of diatoms are known to elicit the production of chemical defense compounds called oxylipins, which are toxic to a wide range of marine organisms. Here we show that (1) the viral infection and lysis of diatoms resulted in oxylipin production; (2) the suite of compounds produced depended on the diatom host and the infecting virus; and (3) the virus-mediated oxylipidome was distinct, in both magnitude and diversity, from oxylipins produced due to stress associated with the growth phase. We used high-resolution accurate-mass mass spectrometry to observe changes in the dissolved lipidome of diatom cells infected with viruses over 3 to 4 days, compared to diatom cells in exponential, stationary, and decline phases of growth. Three host virus pairs were used as model systems: Chaetoceros tenuissimus infected with CtenDNAV; C. tenuissimus infected with CtenRNAV; and Chaetoceros socialis infected with CsfrRNAV. Several of the compounds that were significantly overproduced during viral infection are known to decrease the reproductive success of copepods and interfere with microzooplankton grazing. Specifically, oxylipins associated with allelopathy towards zooplankton from the 6-, 9-, 11-, and 15-lipogenase (LOX) pathways were significantly more abundant during viral lysis. 9-hydroperoxy hexadecatetraenoic acid was identified as the strongest biomarker for the infection of Chaetoceros diatoms. C. tenuissimus produced longer, more oxidized oxylipins when lysed by CtenRNAV compared to CtenDNAV. However, CtenDNAV caused a more statistically significant response in the lipidome, producing more oxylipins from known diatom LOX pathways than CtenRNAV. A smaller set of compounds was significantly more abundant in stationary and declining C. tenuissimus and C. socialis controls. Two allelopathic oxylipins in the 15-LOX pathway and essential fatty acids, arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) were more abundant in the stationary phase than during the lysis of C. socialis. The host–virus pair comparisons underscore the species-level differences in oxylipin production and the value of screening more host–virus systems. We propose that the viral infection of diatoms elicits chemical defense via oxylipins which deters grazing with downstream trophic and biogeochemical effects.more » « less
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