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  1. Abstract

    Small eukaryotic phytoplankton are major contributors to global primary production and marine biogeochemical cycles. Many taxa are thought to be mixotrophic, but quantitative studies of phagotrophy exist for very few. In addition, little is known about consumers of Prochlorococcus, the abundant cyanobacterium at the base of oligotrophic ocean food webs. Here we describe thirty-nine new phytoplankton isolates from the North Pacific Subtropical Gyre (Station ALOHA), all flagellates ~2–5 µm diameter, and we quantify their ability to graze Prochlorococcus. The mixotrophs are from diverse classes (dictyochophytes, haptophytes, chrysophytes, bolidophytes, a dinoflagellate, and a chlorarachniophyte), many from previously uncultured clades. Grazing ability varied substantially, with specific clearance rate (volume cleared per body volume) varying over ten-fold across isolates and six-fold across genera. Slower grazers tended to create more biovolume per prey biovolume consumed. Using qPCR we found that the haptophyte Chrysochromulina was most abundant among the isolated mixotrophs at Station ALOHA, with 76–250 cells mL−1 across depths in the upper euphotic zone (5–100 m). Our results show that within a single ecosystem the phototrophs that ingest bacteria come from many branches of the eukaryotic tree, and are functionally diverse, indicating a broad range of strategies along the spectrum from phototrophy to phagotrophy.

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  2. Abstract

    Persistent nitrogen depletion in sunlit open ocean waters provides a favorable ecological niche for nitrogen-fixing (diazotrophic) cyanobacteria, some of which associate symbiotically with eukaryotic algae. All known marine examples of these symbioses have involved either centric diatom or haptophyte hosts. We report here the discovery and characterization of two distinct marine pennate diatom-diazotroph symbioses, which until now had only been observed in freshwater environments. Rhopalodiaceae diatomsEpithemia pelagicasp. nov. andEpithemia catenatasp. nov. were isolated repeatedly from the subtropical North Pacific Ocean, and analysis of sequence libraries reveals a global distribution. These symbioses likely escaped attention because the endosymbionts lack fluorescent photopigments, havenifHgene sequences similar to those of free-living unicellular cyanobacteria, and are lost in nitrogen-replete medium. Marine Rhopalodiaceae-diazotroph symbioses are a previously overlooked but widespread source of bioavailable nitrogen in marine habitats and provide new, easily cultured model organisms for the study of organelle evolution.

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  3. Abstract

    Viruses span an impressive size range, with genome length varying a thousandfold and virion volume nearly a millionfold. For cellular organisms the scaling of traits with size is a pervasive influence on ecological processes, but whether size plays a central role in viral ecology is unknown. Here, we focus on viruses of aquatic unicellular organisms, which exhibit the greatest known range of virus size. We outline hypotheses within a quantitative framework, and analyse data where available, to consider how size affects the primary components of viral fitness. We argue that larger viruses have fewer offspring per infection and slower contact rates with host cells, but a larger genome tends to increase infection efficiency, broaden host range, and potentially increase attachment success and decrease decay rate. These countervailing selective pressures may explain why a breadth of sizes exist and even coexist when infecting the same host populations. Oligotrophic ecosystems may be enriched in “giant” viruses, because environments with resource‐limited phagotrophs at low concentrations may select for broader host range, better control of host metabolism, lower decay rate and a physical size that mimics bacterial prey. Finally, we describe where further research is needed to understand the ecology and evolution of viral size diversity.

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  4. Abstract

    Mixotrophic nanoflagellates can account for more than half of the bacterivory in the sunlit ocean, yet very little is known about their ecophysiology. Here, we characterize the grazing ecology of an open‐ocean mixotroph in the genusFlorenciella(class Dictyochophyceae). Members of this class were indirectly implicated as major consumers ofProchlorococcusandSynechococcusin the oligotrophic North Pacific Subtropical Gyre, but their phagotrophic capabilities have never been investigated. Our studies showed thatFlorenciellareadily consumedProchlorococcus,Synechococcus, and heterotrophic bacteria, and that the ingested prey relieved nutrient limitations on growth.Florenciellagrew faster (3 d−1) in nitrogen‐deplete medium given sufficient liveSynechococcus, than in nitrogen‐replete K medium (2 d−1), but it did not grow in continuous darkness. Grazing rates were substantially higher under nutrient limitation and showed a hint of diel variability, with rates tending to be highest near the end of the light period. An apparent trade‐off between the maximum clearance rate (5 nLFlorenciella−1h−1) and the maximum ingestion rate (up to ∼ 10 prey cellsFlorenciella−1h−1) across experiments suggests that grazing behavior may also vary in response to prey concentration. If the observed grazing rates are representative of other open‐ocean mixotrophs, their collective activity could account for a significant fraction of the daily cyanobacterial mortality. This study provides essential parameters for understanding the grazing ecology of a common marine mixotroph and the first characterization of mixotrophic nanoflagellate functional responses when feeding on unicellular cyanobacteria, the dominant marine primary producers in the oligotrophic ocean.

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  5. Mixotrophy, the combination of autotrophic and heterotrophic nutrition, is a common trophic strategy among unicellular eukaryotes in the ocean. There are a number of hypotheses about the conditions that select for mixotrophy, and field studies have documented the prevalence of mixotrophy in a range of environments. However, there is currently little evidence for how mixotrophy varies across environmental gradients, and whether empirical patterns support theoretical predictions. Here I synthesize experiments that have quantified the abundance of phototrophic, mixotrophic, and heterotrophic nanoflagellates, to ask whether there are broad patterns in the prevalence of mixotrophy (relative to pure autotrophy and heterotrophy), and to ask whether observed patterns are consistent with a trait-based model of trophic strategies. The data suggest that mixotrophs increase in abundance at lower latitudes, while autotrophs and heterotrophs do not, and that this may be driven by increased light availability. Both mixotrophs and autotrophs increase greatly in productive coastal environments, while heterotrophs increase only slightly. These patterns are consistent with a model of resource competition in which nutrients and carbon can both limit growth and mixotrophs experience a trade-off in allocating biomass to phagotrophy vs. autotrophic functions. Importantly, mixotrophy is selected for under a range of conditions even when mixotrophs experience a penalty for using a generalist trophic strategy, due to the synergy between photosynthetically derived carbon and prey-derived nutrients. For this reason mixotrophy is favored relative to specialist strategies by increased irradiance, while at the same time increased nutrient supply increases the competitive ability of mixotrophs against heterotrophs.

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