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  1. Abstract

    Diverse viruses and their hosts are interconnected through complex networks of infection, which are thought to influence ecological and evolutionary processes, but the principles underlying infection network structure are not well understood. Here we focus on network dimensionality and how it varies across 37 networks of viruses infecting eukaryotic phytoplankton and bacteria. We find that dimensionality is often strikingly low, with most networks being one‐ or two‐dimensional, although dimensionality increases with network richness, suggesting that the true dimensionality of natural systems is higher. Low‐dimensional networks generally exhibit a mixture of host partitioning among viruses and nestededness of host ranges. Networks of bacteria‐infecting and eukaryote‐infecting viruses possess comparable distributions of dimensionality and prevalence of nestedness, indicating that fundamentals of network structure are similar among domains of life and different viral lineages. The relative simplicity of many infection networks suggests that coevolutionary dynamics are often driven by a modest number of underlying mechanisms.

     
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  2. A large fraction of marine primary production is performed by diverse small protists, and many of these phytoplankton are phagotrophic mixotrophs that vary widely in their capacity to consume bacterial prey. Prior analyses suggest that mixotrophic protists as a group vary in importance across ocean environments, but the mechanisms leading to broad functional diversity among mixotrophs, and the biogeochemical consequences of this, are less clear. Here we use isolates from seven major taxa to demonstrate a tradeoff between phototrophic performance (growth in the absence of prey) and phagotrophic performance (clearance rate when consuming Prochlorococcus ). We then show that trophic strategy along the autotrophy-mixotrophy spectrum correlates strongly with global niche differences, across depths and across gradients of stratification and chlorophyll a . A model of competition shows that community shifts can be explained by greater fitness of faster-grazing mixotrophs when nutrients are scarce and light is plentiful. Our results illustrate how basic physiological constraints and principles of resource competition can organize complexity in the surface ocean ecosystem. 
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  3. 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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  4. Abstract

    In sunlit waters, significant predation is performed by unicellular, phagotrophic mixotrophs, that is, predators that also possess plastids. The success of a mixotrophic lifestyle will depend in part on how well mixotrophs acquire prey relative to specialized heterotrophs. Likewise, consequences of mixotrophy for productivity and element cycling will depend on the rate and efficiency at which mixotrophs consume prey biomass relative to heterotrophs. However, trait differences between mixotrophs and heterotrophs are not well characterized. In addition, cell size of mixotrophs varies widely, and constitutive mixotrophs include small flagellates deriving from diverse taxa, while larger species are primarily dinoflagellates. To determine whether similar constraints apply to phagotrophs across this broad range of size and taxa, we compiled 83 measurements of flagellate functional responses and compared maximum clearance rates (Cmax) and maximum ingestion rates (Imax) between trophic modes. We found that the average mixotroph has a 3.7‐fold lowerCmaxand 7.8‐fold lowerImaxthan the average heterotroph, after controlling for cell size. The smaller penalty forCmaxsuggests that relative fitness of mixotrophs will be enhanced under dilute prey concentrations that are common in pelagic ecosystems. We also find that growth efficiency is greater for mixotrophs and for flagellates with lowerCmax, indicating a spectrum of trophic strategies that may be driven by phototrophy vs. phagotrophy allocation as well as fast vs. slow metabolic variation. Allometric scaling shows thatImaxis constrained by a common relationship among dinoflagellates and other taxa, but dinoflagellates achieve a greater volume‐specificCmax. These results should aid in interpreting protistan communities and modeling mixotrophy.

     
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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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  6. 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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