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Long-term stability of picocyanobacteria in the open oceans is maintained by a balance between synchronous division and death on daily timescales. Viruses are considered a major source of microbial mortality, however, current methods to measure infection have significant methodological limitations. Here we describe a method that pairs flow-cytometric sorting with a PCR-based polony technique to simultaneously screen thousands of taxonomically resolved individual cells for intracellular virus DNA, enabling sensitive, high-throughput, and direct quantification of infection by different virus lineages. Under controlled conditions with picocyanobacteria-cyanophage models, the method detected infection throughout the lytic cycle and discriminated between varying infection levels. In North Pacific subtropical surface waters, the method revealed that only a small percentage of Prochlorococcus (0.35–1.6%) were infected, predominantly by T4-like cyanophages, and that infection oscillated 2-fold in phase with the diel cycle. This corresponds to 0.35–4.8% of Prochlorococcus mortality daily. Cyanophages were 2–4-fold more abundant than Prochlorococcus , indicating that most encounters did not result in infection and suggesting infection is mitigated via host resistance, reduced phage infectivity and inefficient adsorption. This method will enable quantification of infection for key microbial taxa across oceanic regimes and will help determine the extent that viruses shape microbial communities and ecosystem level processes.

The rates of cell growth, division, and carbon loss of microbial populations are key parameters for understanding how organisms interact with their environment and how they contribute to the carbon cycle. However, the invasive nature of current analytical methods has hindered efforts to reliably quantify these parameters. In recent years, size-structured matrix population models (MPMs) have gained popularity for estimating division rates of microbial populations by mechanistically describing changes in microbial cell size distributions over time. Motivated by the mechanistic structure of these models, we employ a Bayesian approach to extend size-structured MPMs to capture additional biological processes describing the dynamics of a marine phytoplankton population over the day-night cycle. Our Bayesian framework is able to take prior scientific knowledge into account and generate biologically interpretable results. Using data from an exponentially growing laboratory culture of the cyanobacterium Prochlorococcus , we isolate respiratory and exudative carbon losses as critical parameters for the modeling of their population dynamics. The results suggest that this modeling framework can provide deeper insights into microbial population dynamics provided by size distribution time-series data.

Phytoplankton communities play an important role in marine food webs and biogeochemical cycles. The transition zones between ocean gyres and surrounding waters represent critical ecological boundaries where environmental gradients drive significant shifts in phytoplankton community structure. This study investigates how nutrient availability and temperature shape the size distribution and composition of small phytoplankton (< 5 μ m) communities across the North Pacific Subtropical Gyre (NPSG) boundaries, testing several ecological hypotheses that explain phytoplankton size distribution patterns in relation to environmental variability. We used high-resolution, underway flow cytometry data collected during eight oceanographic cruises from 2016 to 2021 to assess changes in phytoplankton biomass and growth rate across the gyre boundaries. The cyanobacterium Prochlorococcus dominated within the gyre, with biomass ranging from 3.2 to 13.1 μ gC L −1 , and its relative contribution to total phytoplankton biomass varied among cruises (31% to 81%, average 60 ± 16%). Prochlorococcus growth rates were significantly higher within the gyre (0.43 ± 0.18 per day) than outside the gyre (0.28 ± 0.16 per day) (one-sided t-test, p < 0.001). Northward in the gyre, Prochlorococcus biomass and growth rates declined. Some variations in biomass and growth rates were observed southward and eastward, with biomass ranging from 3 to 10 μ gC L −1 and growth rate ranging from 0.2 to 0.6 per day. Outside the NPSG, total phytoplankton biomass increased, with nanoeukaryotes becoming the predominant contributors (up to 71%, 9.1 ± 7.3 μ gC L −1 ). Picoeukaryote biomass also increased outside the gyre (up to 28 ± 12% of total biomass). Nutrient concentrations increased by nearly two orders of magnitude outside the NPSG, coinciding with the shift towards larger phytoplankton. The dominance of Prochlorococcus within the gyre emphasizes its adaptation to oligotrophic conditions, while the shift towards larger size classes outside the gyre likely reflects the relatively higher nutrient availability. The relatively low abundance of Synechococcus even in nutrient-rich regions suggest that that factors beyond nutrient availability, such as grazing, may influence its distribution. These findings have implications for understanding how phytoplankton communities will respond to future changes in oceanographic conditions, such as warming and altered nutrient regimes.

The number of marine environments known to harbor dinitrogen (N₂)-fixing (diazotrophic) microorganisms is increasing, prompting a reassessment of the biogeography of marine diazotrophs and N₂ fixation rates (NFRs). Here, we investigate the diversity, abundance, and activity of diazotrophic microorganisms in the North Pacific Subtropical Gyre (NPSG), a diazotrophic habitat, and the North Pacific Transition Zone (NPTZ), a region characterized by strong physical, chemical, and biological gradients. Samples were collected on two springtime meridional cruises during 2016 and 2017, spanning from 23.5°N to 41.4°N along 158°W. We observed an abrupt decrease in diazotrophic abundances near the southern edge of the NPTZ, which coincided with a salinity front and with ~ 10-fold increase in Synechococcus abundance, but without a concomitant change in phosphate or nitrate concentrations. In NPSG waters south of this diazotrophic boundary, nifH genes and NFRs were consistently detected and diazotrophic communities were dominated by UCYN-A, an uncultivated, symbiotic cyanobacterium (2.8 × 10³ to 1.0 × 10⁶ nifH gene copies L−1). There was a significant positive relationship between quantitative polymerase chain reaction-derived UCYN-A nifH gene abundances and community NFRs in the NPSG, suggesting a large contribution of UCYN-A to community NFRs. In the NPTZ waters to the north, NFRs were low or undetected and nifH genes were rare, with the few detected sequences represented by UCYN-A and noncyanobacterial diazotrophs. The patterns we observed in UCYN-A abundance in the context of local biogeochemistry suggest that the environmental controls of this organism may differ fromthose of cultivated marine cyanobacterial diazotrophs.

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. High-resolution sampling across thousands of kilometres of open ocean reveals a hotspot of viruses at the boundary of major oceanic gyres that, at times, shaped the abundance and biogeography of marine 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. This study shows that a multitrophic community model jointly recapitulates diel rhythms in abundances of Prochlorococcus picocyanobacteria, as well as viral infection, viral abundances and grazer abundances. Model-data integration implies that grazing predominantly controls Prochlorococcus abundances in surface waters of the North Pacific Subtropical Gyre, despite high viral densities.

Diatoms are an important group of eukaryotic phytoplankton, responsible for about 20% of global primary productivity. Study of the functional role of chemical signaling within phytoplankton assemblages is still in its infancy although recent reports in diatoms suggest the existence of chemical-based defense strategies. Here, we demonstrate how the accurate perception of diatom-derived reactive aldehydes can determine cell fate in diatoms. In particular, the aldehyde (2E,4E/Z)-decadienal (DD) can trigger intracellular calcium transients and the generation of nitric oxide (NO) by a calcium-dependent NO synthase-like activity, which results in cell death. However, pretreatment of cells with sublethal doses of aldehyde can induce resistance to subsequent lethal doses, which is reflected in an altered calcium signature and kinetics of NO production. We also present evidence for a DD-derived NO-based intercellular signaling system for the perception of stressed bystander cells. Based on these findings, we propose the existence of a sophisticated stress surveillance system in diatoms, which has important implications for understanding the cellular mechanisms responsible for acclimation versus death during phytoplankton bloom successions.

The 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.