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ABSTRACT Viruses that infect phytoplankton are an integral part of marine ecosystems, but the vast majority of viral diversity remains uncultivated. Here, we introduce four near-complete genomic assemblies of viruses that infect the widespread marine picoeukaryoteMicromonas commoda, doubling the number of reported genomes ofMicromonasdsDNA viruses. All host and virus isolates were obtained from tropical waters of the North Pacific, a first for viruses infecting green algae in the order Mamiellales. Genome length of the new isolates ranges from 205 to 212 kb, and phylogenetic analysis shows that all four are members of the genusPrasinovirus. Three of the viruses form a clade that is adjacent to previously sequencedMicromonasviruses, while the fourth virus is relatively divergent from previously sequenced prasinoviruses. We identified 61 putative genes not previously found in prasinovirus isolates, including a phosphate transporter and a potential apoptosis inhibitor novel to marine viruses. Forty-eight genes in the new viruses are also found in host genome(s) and may have been acquired through horizontal gene transfer. By analyzing the coding sequences of all published prasinoviruses, we found that ~25% of prasinovirus gene content is significantly correlated with host genus identity (i.e.,Micromonas,Ostreococcus, orBathycoccus), and the functions of these genes suggest that much of the viral life cycle is differentially adapted to the three host genera. Mapping of metagenomic reads from global survey data indicates that one of the new isolates, McV-SA1, is relatively common in multiple ocean basins.IMPORTANCEThe genomes analyzed here represent the first viruses from the tropical North Pacific that infect the abundant phytoplankton order Mamiellales. Comparing isolates from the same location demonstrates high genomic diversity among viruses that co-occur and presumably compete for hosts. Comparing all published prasinovirus genomes highlights gene functions that are likely associated with adaptation to different host genera. Metagenomic data indicate these viruses are globally distributed, and one of the novel isolates may be among the most abundant marine viruses. 

Abstract Marine microbes are important in biogeochemical cycling, but the nature and magnitude of their contributions are influenced by their associated viruses. In the presence of a lytic virus, cells that have evolved resistance to infection have an obvious fitness advantage over relatives that remain susceptible. However, susceptible cells remain extant in the wild, implying that the evolution of a fitness advantage in one dimension (virus resistance) must be accompanied by a fitness cost in another dimension. Identifying costs of resistance is challenging because fitness is context‐dependent. We examined the context dependence of fitness costs in isolates of the picophytoplankton genusMicromonasand their co‐occurring dsDNA viruses using experimental evolution. After generating 88 resistant lineages from two ancestralMicromonasstrains, each challenged with one of four distinct viral strains, we found resistance led to a 46% decrease in mean growth rate under high irradiance and a 19% decrease under low. After a year in culture, the experimentally selected lines remained resistant, but fitness costs had attenuated. Our results suggest that the cost of resistance inMicromonasis dependent on environmental conditions and the duration of population adaptation, illustrating the dynamic nature of fitness costs of viral resistance among marine protists. 

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 diatoms Epithemia pelagica sp. nov. and Epithemia catenata sp. 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, have nifH gene 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. 

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. 

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 genus Florenciella (class Dictyochophyceae). Members of this class were indirectly implicated as major consumers of Prochlorococcus and Synechococcus in the oligotrophic North Pacific Subtropical Gyre, but their phagotrophic capabilities have never been investigated. Our studies showed that Florenciella readily consumed Prochlorococcus, Synechococcus, and heterotrophic bacteria, and that the ingested prey relieved nutrient limitations on growth. Florenciella grew faster (3 d−1) in nitrogen‐deplete medium given sufficient live Synechococcus, 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 nL Florenciella−1 h−1) and the maximum ingestion rate (up to ∼ 10 prey cells Florenciella−1 h−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. 

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.