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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. 

Viruses infecting aquatic microbes vary immensely in size, but the ecological consequences of virus size are poorly understood. Here we used a unique suite of diverse phytoplankton strains and their viruses, all isolated from waters around Hawai'i, to assess whether virus size affects the suppression of host populations. We found that small viruses of diverse genome type (3–24 kb genome size, 23–70 nm capsid diameter) have very similar effects on host populations, suppressing hosts less strongly and for a shorter period of time compared to large double‐stranded DNA viruses (214–1380 kb, 112–386 nm). Suppressive effects of larger viruses were more heterogeneous, but most isolates reduced host populations by many orders of magnitude, without recovery over the ~ 25‐d experiments. Our results suggest that disparate lineages of viruses may have ecological consequences that are predictable in part based on size, and that ecosystem impacts of viral infection may vary with the size structure of the viral community. 

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. 

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. 

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. 

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.