Seasonal shifts in phytoplankton accumulation and loss largely follow changes in mixed layer depth, but the impact of mixed layer depth on cell physiology remains unexplored. Here, we investigate the physiological state of phytoplankton populations associated with distinct bloom phases and mixing regimes in the North Atlantic. Stratification and deep mixing alter community physiology and viral production, effectively shaping accumulation rates. Communities in relatively deep, early-spring mixed layers are characterized by low levels of stress and high accumulation rates, while those in the recently shallowed mixed layers in late-spring have high levels of oxidative stress. Prolonged stratification into early autumn manifests in negative accumulation rates, along with pronounced signatures of compromised membranes, death-related protease activity, virus production, nutrient drawdown, and lipid markers indicative of nutrient stress. Positive accumulation renews during mixed layer deepening with transition into winter, concomitant with enhanced nutrient supply and lessened viral pressure.
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Abstract Heterotrophic bacteria in the surface ocean play a critical role in the global carbon cycle and the magnitude of this role depends on their growth rates. Although methods for determining bacterial community growth rates based on incorporation of radiolabeled thymidine and leucine are widely accepted, they are based on a number of assumptions and simplifications. We sought to independently assess these methods by comparing bacterial growth rates to turnover rates of bacterial membranes using previously published methods in a range of open‐ocean settings. We found that turnover rates for heterotrophic bacterial phospholipids averaged 0.80 ± 0.35 d−1. This was supported by independent measurements of turnover rates of a membrane‐bound pigment in photoheterotrophic bacteria, bacteriochlorophyll
a (0.85 ± 0.09 d−1). By contrast, bacterial growth rates measured by uptake of radiolabeled thymidine and leucine were 0.12 ± 0.08 d−1, well within the range expected from the literature. We explored whether the discrepancies between phospholipid turnover rates and bacterial growth rate could be explained by membrane recycling/remodeling and other factors, but were left to conclude that the radiolabeled thymidine and leucine incorporation methods substantially underestimated actual bacterial growth rates. We use a simple model to show that the faster bacterial growth rates we observed can be accommodated within the constraints of the microbial carbon budget if bacteria are smaller than currently thought, grow with greater efficiency, or some combination of these two factors. -
Abstract Emiliania huxleyi is a globally important marine phytoplankton that is routinely infected by viruses. Understanding the controls on the growth and demise of E. huxleyi blooms is essential for predicting the biogeochemical fate of their organic carbon and nutrients. In this study, we show that the production of nitric oxide (NO), a gaseous, membrane-permeable free radical, is a hallmark of early-stage lytic infection in E. huxleyi by Coccolithoviruses, both in culture and in natural populations in the North Atlantic. Enhanced NO production was detected both intra- and extra-cellularly in laboratory cultures, and treatment of cells with an NO scavenger significantly reduced viral production. Pre-treatment of exponentially growing E. huxleyi cultures with the NO donor S-nitroso-N-acetylpenicillamine (SNAP) prior to challenge with hydrogen peroxide (H2O2) led to greater cell survival, suggesting that NO may have a cellular antioxidant function. Indeed, cell lysates generated from cultures treated with SNAP and undergoing infection displayed enhanced ability to detoxify H2O2. Lastly, we show that fluorescent indicators of cellular ROS, NO, and death, in combination with classic DNA- and lipid-based biomarkers of infection, can function as real-time diagnostic tools to identify and contextualize viral infection in natural E. huxleyi blooms.
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Abstract Marine sinking particles transport carbon from the surface and bury it in deep‐sea sediments, where it can be sequestered on geologic time scales. The combination of the surface ocean food web that produces these particles and the particle‐associated microbial community that degrades them creates a complex set of variables that control organic matter cycling. We use targeted metabolomics to characterize a suite of small biomolecules, or metabolites, in sinking particles and compare their metabolite composition to that of the suspended particles in the euphotic zone from which they are likely derived. These samples were collected in the South Atlantic subtropical gyre, as well as in the equatorial Atlantic region and the Amazon River plume. The composition of targeted metabolites in the sinking particles was relatively similar throughout the transect, despite the distinct oceanic regions in which they were generated. Metabolites possibly derived from the degradation of nucleic acids and lipids, such as xanthine and glycine betaine, were an increased mole fraction of the targeted metabolites in the sinking particles relative to surface suspended particles, while algal‐derived metabolites like the osmolyte dimethylsulfoniopropionate were a smaller fraction of the observed metabolites on the sinking particles. These compositional changes are shaped both by the removal of metabolites associated with detritus delivered from the surface ocean and by production of metabolites by the sinking particle‐associated microbial communities. Furthermore, they provide a basis for examining the types and quantities of metabolites that may be delivered to the deep sea by sinking particles.
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Summary Coccolithoviruses (EhVs) are large, double‐stranded DNA‐containing viruses that infect the single‐celled, marine coccolithophoreEmiliania huxleyi . Given the cosmopolitan nature and global importance ofE. huxleyi as a bloom‐forming, calcifying, photoautotroph,E. huxleyi –EhV interactions play a key role in oceanic carbon biogeochemistry. Virally‐encoded glycosphingolipids (vGSLs) are virulence factors that are produced by the activity of virus‐encoded serine palmitoyltransferase (SPT). Here, we characterize the dynamics, diversity and catalytic production of vGSLs in an array of EhV strains in relation to their SPT sequence composition and explore the hypothesis that they are a determinant of infectivity and host demise. vGSL production and diversity was positively correlated with increased virulence, virus replication rate and lytic infection dynamics in laboratory experiments, but they do not explain the success of less‐virulent EhVs in natural EhV communities. The majority of EhV‐derived SPT amplicon sequences associated with infected cells in the North Atlantic derived from slower infecting, less virulent EhVs. Our lab‐, field‐ and mathematical model‐based data and simulations support ecological scenarios whereby slow‐infecting, less‐virulent EhVs successfully compete in North Atlantic populations ofE. huxleyi , through either the preferential removal of fast‐infecting, virulent EhVs during active infection or by having access to a broader host range.