Abstract Viral lysis fuels the microbial loop by enhancing organic matter recycling (via the viral shunt) and can redirect organic matter toward export (via the viral shuttle). However, the global impact of viral infection mediated by shunt and shuttle pathways remains unclear. Here, we implemented viral infection and lysis processes in a global ocean ecosystem model, including a single phytoplankton (representing Prochlorococcus ), virus (representing cyanophage), and nanozooplankton. Despite low but plausible levels of viral infection, high shunt efficiencies generated enhanced-productivity regions covering up to approximately one-half of the global ocean. For lower viral shunt efficiencies, the enhanced-productivity regions contracted abruptly, accompanied by steady declines in productivity. Viral-mediated increases in primary productivity reduced the extent of tropical oligotrophic regions at high shunt efficiencies, while lower efficiencies expanded oligotrophic areas. These results provide a path forward to developing predictive models of how viral infection and the fate of cellular lysates shape global ocean ecosystems.

Abstract Viruses and grazers are fundamental agents of mortality in the oceans, impacting phytoplankton populations and organic matter cycling. Although viruses and grazers co-occur in nature, they are typically studied in isolation in laboratory experiments, limiting our understanding of their combined ecosystem impacts. Here, using a simplified ecosystem approach, we investigated individual and combined effects of the T7-like cyanopodovirus, P-SSP7, and the protistan grazer, Paraphysomonas bandaiensis, on the abundant marine cyanobacterium, Prochlorococcus MED4, and co-occurring non-photosynthetic heterotrophic bacteria (bacteria from here on). We observed that, individually, viruses and grazers caused substantial Prochlorococcus mortality. Viral lysis also triggered increases in damaged Prochlorococcus cells, dissolved organic matter release, and bacterial growth, while grazing reduced bacterial abundances. When grazers and viruses were combined, Prochlorococcus mortality was lower than expected from the sum of their individual effects. Contrary to expectations, this reduced Prochlorococcus mortality did not result in fewer viruses or grazers. Instead, virus-grazer- Prochlorococcus interplay resulted in greater virus production, maintenance of grazer growth, and a dramatic increase in particle aggregation. Our results reveal trophic cooperation and efficiency in which competition between viruses and grazers was likely mitigated, with virus progeny production enhanced by grazers, and grazer growth sustained through a shift to alternative food sources (bacteria, damaged cells, aggregates) secondarily derived from Prochlorococcus following viral lysis. The synergistic enhancement of particle aggregation via grazer-virus-phytoplankton interplay observed with the small buoyant Prochlorococcus phytoplankter underscores the importance of food web interactions for the flow of phytoplankton-fixed carbon within, and export from, the photic zone. Significance Viruses and grazers both use phytoplankton as a resource for reproduction. In a simplified experimental system with Prochlorococcus , an important primary producer in the oceans, we found that the interplay between viruses and grazers led to reduced mortality of Prochlorococcus . Despite this reduced mortality, virus-grazer interactions resulted in elevated virus production and a dramatic increase in organic matter aggregation. Furthermore, grazer abundance was not affected by this interplay, likely due to the transfer of organic matter from Prochlorococcus to bacteria and aggregates, which the grazers could consume as alternative food sources. These findings provide insights into the complexity of ecosystem interactions and how they impact the fate of organic matter fixed by phytoplankton in the oceans.

Abstract Virus-induced mortality influences plankton biogeography, community structure, and ocean elemental cycles. However, quantification of virus-induced impacts remains challenging and often limited in scope. An alternative to explicit inclusion of viral dynamics in biogeochemical models is to represent viral effects implicitly, by assuming that mortality increases quadratically with cell or biomass density. Using 1D and 3D configurations of a nutrient-phytoplankton-zooplankton-virus-detritus (NPZVD) model, we ask whether the implicit quadratic mortality assumption captures patterns of virus-induced mortality, and its impact on biomass and primary production. The 1D water-column configuration shows that, at the onset of the spring bloom, the quadratic, implicit representation imposes viral losses on phytoplankton density instantaneously, which limits spring bloom formation. This is in contrast to the explicit representation, which allows initial bloom formation to proceed unhampered initially, but imposes a far stronger viral mortality later in the year driven by high rates of host-virus contact due to high phytoplankton and viral densities that take time to accumulate. By comparison to the implicit model, explicit resolution of viruses within the 3D global model shows strong potential for viruses to prematurely terminate phytoplankton blooms. Biogeochemical models would therefore benefit from explicit representation of viral infection insofar as models can be developed that adequately recapitulate in situ observations. Key Points Global model reveals significant spatial heterogeneity arising from explicit, rather than implicit, representation of viruses Implicit representation of viral dynamics fails to capture the potential for viruses to terminate phytoplankton blooms Biogeochemical models require explicit representation of viruses to adequately simulate their effect on marine systems

Phage-induced lysis of bacteria transforms population dynamics, community structure, and ecosystem functioning. Scaling up infected cell fate to quantify population- and ecosystem-scale impacts requires estimates of viral life-history traits, including underlying heterogeneity in the timing, efficiency, and outcome of lytic infections. However, the variability of lysis-associated phage traits remains poorly characterized. Here, we infer single-cell heterogeneity in lysis-associated traits for an ecologically relevant system: Syn9, a T4-like cyanophage infecting Synechococcus strain WH8109, a representative of globally abundant marine cyanobacteria. We estimate the heterogeneous distribution of latent period and burst size using a nonlinear model of infection dynamics applied to population-scale time-series data. We then validate our inference approach using a single-cell assay-demonstrating the feasibility of inferring phage trait heterogeneity from population data even in the absence of single-cell experiments. The variation in Syn9's latent period exceeds that previously found in coliphages and reinforces the limitations of representing viral traits with a single value. Moreover, by partitioning lytic events via the inferred heterogeneous latent period distribution, we show that realized burst size variability is largely explained by differences in latent period, providing a path forward to measure and integrate trait (co)variation into population and ecosystem models.

Photosynthetic microorganisms are responsible for primary production at the base of the marine food web and influence global biogeochemistry. Their growth is balanced by mortality processes, including zooplankton grazing and viral lysis. These predators coexist despite competing for the same microorganisms. Here, we develop a community model of photosynthetic microorganisms, grazers and viruses that incorporates elemental quotas and is suitable for ocean ecosystem models. We evaluate the extent to which coexistence is facilitated by: (i) explicit infected phytoplankton; (ii) heterogeneity in susceptibility to viral infection; and (iii) higher-order mortality for the predators. We show a trade-off between the virus latent period and virulence in facilitating coexistence. The latent period generates oscillations that reduce the growth rate of the free virus, promoting coexistence. Heterogeneity in susceptibility supports coexistence through resource partitioning, while higher-order mortality widens the coexistence regime. The model outcomes are sensitive to viral life history traits, including the percentage of infected cells and the balance between virally- and zooplankton-induced mortality. Leveraging algebraic model equilibria, we identify parameter combinations that yield realistic ecological properties in simplified epipelagic environments. Our models suggest that efforts to embed virus dynamics in ocean ecosystem models should include moderate to strong resistance to viral infection.

Cyanobacteria play a significant role in global biogeochemical cycles, including carbon fixation and oxygen production. Among them, marine picocyanobacteria Prochlorococcus and Synechococcus constitute the most numerically abundant group of photosynthetic organisms on Earth. They are dominant in oligotrophic regions and contribute a quarter of primary production in the ocean. Picocyanobacterial distribution depends on abiotic factors, e.g. light, temperature, and nutrients, as well as biotic mortality factors, such as grazers and viral infection. Viruses also impact the diversity of picocyanobacteria during their coevolution. Infection of cyanobacteria by phages ends in lysis and release of organic matter from cells to the water column. The T7-like cyanophage family is one of two main virus families infecting marine picocyanobacteria. Two groups of T7-like cyanophages were known until recently: clades A and B. They have various distribution, infection properties and patterns, resulting in differential impacts on picocyanobacterial populations. In 2023 a new group of T7-like cyanophages was discovered, and was named clade C. However, only two genotypes of the novel group were known, both isolated on Prochlorococcus. In this study we investigated the diversity within the new group using assembled environmental sequences. We also estimated the relative abundance and infection of this group and compared them with other T7-like cyanophages clades along a transect in the North Pacific Ocean and over the spring period or from winter mixing to summer stratification in the Red Sea. For this we used viromic and cellular metagenomic data to determine relative abundance of free-living viruses and gain an indication of infection, respectively. We found that the new group actually consists of two distinct clades, which we renamed as clades C and D. Clade D is more diverse than clade C. In the North Pacific Ocean both clades were relatively more abundant in the North Pacific Subtropical Gyre and decreased towards the north. In some samples clade D recruited more than 40% of T7-like cyanophage viromic reads. In the Red Sea the relative abundance of both clades increased towards the summer. In both regions clade D was generally more abundant that clade C, and the abundances of clades C and D followed the abundances of Prochlorococcus. This study provides new insights into the diversity, spatial distribution and seasonal dynamics of two new clades of T7-like cyanophages. It demonstrates that clade D could be an important viral group impacting primary production and biogeochemical cycles in the oligotrophic oceans.

ABSTRACTCyanobacterial distributions are shaped by abiotic factors including temperature, light and nutrient availability as well as biotic factors such as grazing and viral infection. In this study, we investigated the abundances of T4‐like and T7‐like cyanophages and the extent of picocyanobacterial infection in the cold, high‐nutrient‐low‐chlorophyll, sub‐Antarctic waters of the southwest Pacific Ocean during austral spring. Synechococcus was the dominant picocyanobacterium, ranging from 4.7 × 103 to 1.2 × 105 cells∙mL−1, while Prochlorococcus abundances were relatively low overall, ranging from 1.0 × 103 to 3.9 × 104 cells∙mL−1. Using taxon‐specific, single‐virus and single‐cell polony methods, we found that cyanophages were on average 15‐fold, and up to 50‐fold, more abundant than cyanobacteria in these waters. T4‐like cyanophages (ranging from 1.7 × 105 to 6.5 × 105 phage·mL−1) were 2.7‐fold more abundant than T7‐like cyanophages (ranging from 3.1 × 104 to 2.8 × 105 phage·mL−1). Picocyanobacteria were primarily infected by T4‐like cyanophages with more Synechococcus (4.8%–12.1%) infected than Prochlorococcus (2.5%–6.2%), whereas T7‐like cyanophages infected less than 1% of both genera. These infection levels translated to daily mortality in the range of 5.7%–26.2% and 2.9%–14.3% of the standing stock of Synechococcus and Prochlorococcus, respectively. Our findings suggest that T4‐like cyanophages are significant agents of cyanobacterial mortality in the cold, low‐iron, sub‐Antarctic waters of the South Pacific Ocean.

Subsurface oxygen maxima (SOMs) occur directly beneath the mixed layer of stratified water columns across oligotrophic open ocean basins and have been associated with physical transport processes and localized increases in phytoplankton net primary productivity (NPP). We explore the hypothesis that viral lysis (i.e., the 'viral shunt') increases nutrient recycling and enhances NPP, supporting SOM formation in stratified water columns, focusing on a recurring SOM at the Bermuda Atlantic Time Series (BATS) in the Sargasso Sea. Reanalysis of historical BATS data showed enhanced Prochlorococcus and virus-like particle abundances associated with SOMs. Instances of high rates of primary and secondary production observed with oxygen supersaturation further implicate a biological mechanism for SOM formation. Leveraging metatranscriptomes, metaviromes, and polony-based data collected during a Lagrangian cruise (October 2019), we link the viral shunt to SOMs, including evidence of elevated cyanophage abundance and infection of Prochlorococcus, and transcriptomic evidence of increased organic matter uptake (i.e., catabolic activity) by copiotrophic bacteria. Cruise data also showed Prochlorococcus nitrogen metabolism transcripts consistent with increased responsiveness to bacterial remineralization. These findings illustrate the biogeochemical impacts of enhanced viral lysis in marine systems, including the potential role of the viral shunt in facilitating SOM formation in the oligotrophic oceans.

IntroductionGrazing on picoplankton by microbial eukaryotes is a fundamental process within aquatic food webs, particularly in oligotrophic regions that are typically dominated by picophytoplankton. Remarkably, classical methods that have been used for decades to measure this process in the field have rarely been evaluated under controlled laboratory conditions where true rates of prey mortality can be quantified and compared to experimental results. This study evaluated two commonly used field techniques to estimate phytoplankton mortality rates by microbial consumers, the dilution technique and the disappearance of fluorescently labeled bacteria (FLB).MethodsAn elaborate laboratory experiment was first conducted comparing picophytoplankton mortality rates measured using these two techniques to rates observed directly in culture based on changes in prey abundance, using the cyanobacterium, Prochlorococcus, as prey for a nanozooplanktonic grazer, Paraphysomonas bandaiensis. Secondly, a field experiment was performed in the North Pacific Subtropical Gyre off Hawai’i to compare the mortality rates estimated by the two methods.ResultsSummed across multiple treatments in the laboratory, mortality rates estimated by FLB disappearance displayed high variability and on average underestimated observed mortality rates by ∼27%. The dilution technique also underestimated observed mortality rates (by ∼54%) but displayed lower variance (yielding an approximately 27% difference between the two methods). In contrast to laboratory results, field experiments resulted in an order of magnitude difference between grazer-mediated mortality rates using the two methods.DiscussionOur laboratory results revealed that both methods yielded reasonable albeit somewhat underestimated mortality rates in the laboratory setup, while differences between the two methods in our field studies implied that the underlying assumptions of one or both methods were not met. These findings advocate for caution in interpreting quantitative assessments of protistan-based mortality rates using these long-used approaches.

Phage-induced lysis of bacteria transforms population dynamics, community structure, and ecosystem functioning. Scaling up infected cell fate to ecosystem-scale impacts requires quantitative estimates of viral life history traits, including underlying heterogeneity in the timing, efficiency, and outcome of lytic infections. Here, we apply a nonlinear model of phage-bacteria infection dynamics to infer single-cell heterogeneity of phage-induced lysis from population-scale time series. We evaluate this inference approach in an ecologically relevant system: Syn9, a T4-like cyanophage infecting Synechococcus strain WH8109, a representative of globally abundant marine cyanobacteria. The model infers heterogeneous distributions of latent period and burst size that were subsequently validated using a single-cell assay. We find observed latent period variation exceeds that found in coliphage with holin lysis systems and that burst size variability is largely explained due to latent period variation. These findings demonstrate the feasibility of inferring phage trait heterogeneity from population data in ecologically relevant systems even in the absence of single-cell experiments. ### Competing Interest Statement The authors have declared no competing interest.

Thioredoxins are ubiquitous redox proteins that are found in all domains of life. These conserved proteins are also found in many phages, including marine cyanophages that infect the ecologically important marine cyanobacteria. However, their role in phage infection is not known. Cyanophages also carry many small genes lacking homology to known functional domains. Whether these have a functional role or not remains unknown. Here, we explore the distribution and role of a cyanophage thioredoxin ( trxA ), and that of a small gene directly downstream of it ( g26 ), in phage infection. For this we used the T7-like cyanophage, Syn5, which infects an open-ocean marine Synechococcus strain, WH8109. We found that thioredoxin genes are common in phage genomes, including in cyanophages. The g26 gene, however, is restricted in it distribution to the cyanophages. The cyanophage thioredoxin is catalytically active and it increases phage DNA replication, progeny production and competitive fitness. It also negatively impacts host growth. The g26 gene product is translationally coupled to, and thus dependent on, translation of the thioredoxin gene. This gene itself significantly increases phage virulence and fitness, yet reduces burst size. Our findings demonstrate that cyanophage thioredoxins impact phage fitness and infection physiology and that small viral genes with no homology to known genes can play an important role in the infection process. These findings provide insights into the importance of unusual genes in phage genomes and show that they are likely to play an important role in the interactions between abundant cyanobacteria and cyanophages in ocean ecosystems. ### Competing Interest Statement The authors have declared no competing interest.

Synechococcus is a significant primary producer in the oceans, coexisting with cyanophages, which are important agents of mortality. Bacterial resistance against phage infection is a topic of significant interest, yet little is known for ecologically relevant systems. Here we use exogenous gene expression and gene disruption to investigate mechanisms underlying intracellular resistance of marine Synechococcus WH5701 to the Syn9 cyanophage. The restriction–modification and Gabija defence systems possessed by Synechococcus WH5701 did not contribute to resistance. Instead, resistance was primarily driven by insufficient levels of LeuTAA tRNA, preventing translation of key phage genes in a passive, intracellular mode of resistance. Restoring cellular tRNA expression rendered the cyanobacterium sensitive to infection. We propose an evolutionary scenario whereby changes in cell codon usage, acquisition of tRNAs by the phage and loss of cell and phage tRNA expression resulted in an effective means of resistance, highlighting the dynamic interplay between bacteria and phages in shaping their co-evolutionary trajectories. Depletion of host LeuTAA tRNA levels prevents the translation of key cyanophage genes during infection and represents a passive, intracellular mode of resistance with implications for co-evolution.

Marine picocyanobacteria are abundant photosynthetic organisms of global importance. They coexist in the ocean with cyanophages-viruses that infect cyanobacteria. Cyanophages carry many auxiliary metabolic genes acquired from their hosts that are thought to redirect host metabolism for the phage's benefit1-5. One such gene is nblA, which is present in multiple cyanophage families2,6-8. Under nutrient deprivation cyanobacterial NblA is responsible for inducing proteolytic degradation of the phycobilisome9-11, the large cyanobacterial photosynthetic light-harvesting complex. This increases the pool of amino acids available for essential tasks11, serving as a survival mechanism12. Ectopic expression of different cyanophage nblA genes results in host pigment protein degradation6,8,13. However, the benefit of the virus-encoded NblA for cyanophages and the broader impact on the host are unclear. Here, using a recently developed genetic manipulation system for marine cyanophages14, we reveal that viral NblA significantly accelerates the cyanophage infection cycle, directs degradation of the host phycobilisome and other proteins, and reduces host photosynthetic light-harvesting efficiency. Metagenomic analysis revealed that cyanophages carrying nblA are widespread in the oceans and comprise 35% and 65% of oceanic T7-like cyanophages in surface and deep photic zones, respectively. Our results show a large benefit of NblA to the cyanophage, while it exerts a negative effect on the host photosynthetic apparatus and host photosynthesis. These findings suggest that cyanophage NblA has an adverse global impact on light harvesting by oceanic picocyanobacteria.

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers in this environment function as the predominant top-down factor despite high standing viral particle densities. The model-data fits also reveal the ecological relevance of light-dependent viral traits and non-canonical factors to cellular loss. Finally, we leverage sensitivity analyses to demonstrate how variation in life history traits across distinct oceanic contexts, including variation in viral adsorption and grazer clearance rates, can transform the quantitative and even qualitative importance of top-down controls in shaping Prochlorococcus population dynamics.

Marine picocyanobacteria are abundant photosynthetic organisms of global importance. They coexist in the ocean with cyanophages, viruses that infect cyanobacteria. Cyanophages carry many auxiliary metabolic genes acquired from their hosts that are thought to redirect host metabolism for the phage's benefit 1-5. One such gene is nblA which is present in multiple cyanophage families 2, 6-9. Under nutrient deprivation the cyanobacterial NblA is responsible for inducing proteolytic degradation of the phycobilisome 10-12, the large cyanobacterial photosynthetic light harvesting complex. This increases the pool of amino acids available for essential tasks 12, serving as a survival mechanism 13. Ectopic expression of different cyanophage nblA genes results in host pigment protein degradation 9,7,6. However, the benefit of the cyanophage-encoded NblA for the cyanophage and the broader impact on the host are unknown. Here, using a recently developed genetic manipulation system for cyanophages 14, we reveal that cyanophage NblA significantly accelerates the cyanophage infection cycle, directs degradation of the host phycobilisome and other photosynthetic proteins and reduces host photosynthetic light harvesting efficiency. Furthermore, metagenomic analysis revealed that cyanophages carrying nblA are widespread in the oceans and compose 35% and 65% of oceanic T7-like cyanophages in the surface and deep photic zones, respectively. Our results show a large benefit of the nblA gene to the cyanophage while exerting a negative effect on the host photosynthetic apparatus and host photosynthesis. These findings suggest that nblA-encoding cyanophages have a global effect on the amount of light harvested by oceanic picocyanobacteria. ### Competing Interest Statement The authors have declared no competing interest.

Viruses are abundant in the ocean and influence both the composition of marine communities and biogeochemical cycles. Despite their high abundance, production rates of distinct virus taxa in the environment are largely unknown. Here, we investigated production dynamics of T4-like cyanophages and compared them to those of the total dsDNA virioplankton community in two adjacent eddies of opposite polarity in the North Pacific Subtropical Gyre. Virioplankton production rates were 3-fold higher in the cyclonic than in the anticyclonic eddy, potentially due to higher metabolic activity of their bacterial hosts in the cyclone, and had similar virus production rates during the day and night in the cyclone. In contrast, T4-like cyanophages had similar production rates in the two eddies but showed approximately 4-fold higher production rates at night than during the day, potentially due to a combination of greater infection, increased burst size and more cyanophages completing their infection cycle at night. These findings suggest that virioplankton community production is affected more by spatially differentiated environmental conditions while T4-like cyanophage production is more affected over the diel cycle. Differences in production for the T4-like cyanophages relative to the virioplankton community indicate that spatial variability at the mesoscale differentially impact distinct components of the virioplankton.

Siderophores are strong iron-binding molecules produced and utilized by microbes to acquire the limiting nutrient iron (Fe) from their surroundings. Despite their importance as a component of the iron-binding ligand pool in seawater, data on the distribution of siderophores and the microbes that use them are limited. Here we measured the concentrations and types of dissolved siderophores during two cruises in April 2016 and June 2017 that transited from the iron-replete, low-macronutrient North Pacific Subtropical Gyre (NPSG) through the North Pacific Transition Zone (NPTZ) to the iron-deplete, high-macronutrient North Pacific Subarctic Frontal Zone (SAFZ). Surface siderophore concentrations in 2017 were higher in the NPTZ (4.0 – 13.9 pM) than the SAFZ (1.2 – 5.1 pM), which may be partly attributed to stimulated siderophore production by environmental factors such as dust-derived iron concentrations (up to 0.51 nM). Multiple types of siderophores were identified on both cruises, including ferrioxamines, amphibactins and iron-free forms of photoreactive siderophores, which suggest active production and use of diverse siderophores across latitude and depth. Additionally, the widespread genetic potential for siderophore biosynthesis and uptake across latitude and the variability in the taxonomic composition of bacterial communities that transcribe putative ferrioxamine, amphibactin and salmochelin transporter genes at different latitudes suggest that particular microbes actively produce and use siderophores, altering siderophore distributions and the bioavailability of iron across the North Pacific.

Ocean ecosystems are inhabited by a diverse set of viruses that impact microbial mortality and evolution. However, the distribution and abundances of specific viral lineages, particularly those from the large bank of rare viruses, remains largely unknown. Here, we assessed the diversity and abundance of the TIM5-like cyanophages. The sequencing of three new TIM5-like cyanophage genomes and environmental amplicons of a signature gene from the Red Sea revealed highly conserved gene content and sequence similarity. We adapted the polony method, a solid-phase polymerase chain reaction assay, to quantify TIM5-like cyanophages during three 2000 km expeditions in the Pacific Ocean and four annual cycles in the Red Sea. TIM5-like cyanophages were widespread, detected at all latitudes and seasons surveyed throughout the photic zone. Yet they were generally rare, ranging between <100 and 4000 viruses·ml-1 . Occasional peaks in abundance of 10- to 100-fold were observed, reaching 71,000 viruses·ml-1 . These peaks were ephemeral and seasonally variable in the Red Sea. Infection levels, quantified during one such peak, were very low. These characteristics of low diversity and abundance, as well as variable outbreaks, distinguishes the TIM5-like lineage from other major cyanophage lineages and illuminates that rare virus lineages can be persistent and widespread in the oceans.

Environmental virus communities are highly diverse. However, the infection physiology underlying the evolution of diverse phage lineages and their ecological consequences are largely unknown. T7-like cyanophages are abundant in nature and infect the marine unicellular cyanobacteria, Synechococcus and Prochlorococcus , important primary producers in the oceans. Viruses belonging to this genus are divided into two distinct phylogenetic clades: clade A and clade B. These viruses have narrow host-ranges with clade A phages primarily infecting Synechococcus genotypes, while clade B phages are more diverse and can infect either Synechococcus or Prochlorococcus genotypes. Here we investigated infection properties (life history traits) and environmental abundances of these two clades of T7-like cyanophages. We show that clade A cyanophages have more rapid infection dynamics, larger burst sizes and greater virulence than clade B cyanophages. However, clade B cyanophages were at least 10-fold more abundant in all seasons, and infected more cyanobacteria, than clade A cyanophages in the Red Sea. Models predicted that steady-state cyanophage abundances, infection frequency, and virus-induced mortality, peak at intermediate virulence values. Our findings indicate that differences in infection properties are reflected in virus phylogeny at the clade level. They further indicate that infection properties, together with differences in subclade diversity and host repertoire, have important ecological consequences with the less aggressive, more diverse virus clade having greater ecological impacts.

The photosynthetic picocyanobacteria Prochlorococcus and Synechococcus are models for dissecting how ecological niches are defined by environmental conditions, but how interactions with bacteriophages affect picocyanobacterial biogeography in open ocean biomes has rarely been assessed. We applied single-virus and single-cell infection approaches to quantify cyanophage abundance and infected picocyanobacteria in 87 surface water samples from five transects that traversed approximately 2,200 km in the North Pacific Ocean on three cruises, with a duration of 2–4 weeks, between 2015 and 2017. We detected a 550-km-wide hotspot of cyanophages and virus-infected picocyanobacteria in the transition zone between the North Pacific Subtropical and Subpolar gyres that was present in each transect. Notably, the hotspot occurred at a consistent temperature and displayed distinct cyanophage-lineage composition on all transects. On two of these transects, the levels of infection in the hotspot were estimated to be sufficient to substantially limit the geographical range of Prochlorococcus . Coincident with the detection of high levels of virally infected picocyanobacteria, we measured an increase of 10–100-fold in the Synechococcus populations in samples that are usually dominated by Prochlorococcus . We developed a multiple regression model of cyanophages, temperature and chlorophyll concentrations that inferred that the hotspot extended across the North Pacific Ocean, creating a biological boundary between gyres, with the potential to release organic matter comparable to that of the sevenfold-larger North Pacific Subtropical Gyre. Our results highlight the probable impact of viruses on large-scale phytoplankton biogeography and biogeochemistry in distinct regions of the oceans.