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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.

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.

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 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.

Up to half of marine N losses occur in oxygen-deficient zones (ODZs). Organic matter flux from productive surface waters is considered a primary control on N 2 production. Here we investigate the offshore Eastern Tropical North Pacific (ETNP) where a secondary chlorophyll a maximum resides within the ODZ. Rates of primary production and carbon export from the mixed layer and productivity in the primary chlorophyll a maximum were consistent with oligotrophic waters. However, sediment trap carbon and nitrogen fluxes increased between 105 and 150 m, indicating organic matter production within the ODZ. Metagenomic and metaproteomic characterization indicated that the secondary chlorophyll a maximum was attributable to the cyanobacterium Prochlorococcus , and numerous photosynthesis and carbon fixation proteins were detected. The presence of chemoautotrophic ammonia-oxidizing archaea and the nitrite oxidizer Nitrospina and detection of nitrate oxidoreductase was consistent with cyanobacterial oxygen production within the ODZ. Cyanobacteria and cyanophage were also present on large (>30 μm) particles and in sediment trap material. Particle cyanophage-to-host ratio exceeded 50, suggesting that viruses help convert cyanobacteria into sinking organic matter. Nitrate reduction and anammox proteins were detected, congruent with previously reported N 2 production. We suggest that autochthonous organic matter production within the ODZ contributes to N 2 production in the offshore ETNP.

Marine cyanobacteria of the genera Synechococcus and Prochlorococcus are the most abundant photosynthetic organisms on earth, spanning vast regions of the oceans and contributing significantly to global primary production. Their viruses (cyanophages) greatly influence cyanobacterial ecology and evolution. Although many cyanophage genomes have been sequenced, insight into the functional role of cyanophage genes is limited by the lack of a cyanophage genetic engineering system. Here, we describe a simple, generalizable method for genetic engineering of cyanophages from multiple families, that we named REEP for REcombination, Enrichment and PCR screening. This method enables direct investigation of key cyanophage genes, and its simplicity makes it adaptable to other ecologically relevant host-virus systems. T7-like cyanophages often carry integrase genes and attachment sites, yet exhibit lytic infection dynamics. Here, using REEP, we investigated their ability to integrate and maintain a lysogenic life cycle. We found that these cyanophages integrate into the host genome and that the integrase and attachment site are required for integration. However, stable lysogens did not form. The frequency of integration was found to be low in both lab cultures and the oceans. These findings suggest that T7-like cyanophage integration is transient and is not part of a classical lysogenic cycle.

Light-driven forcing of cellular growth processes in the upper mixed layer of the ocean fuels primary and secondary production at the base of marine food webs. Motivated by high-frequency measurements taken by Lagrangian sampling in the North Pacific Subtropical Gyre (NPSG), we developed a hierarchical set of multi-trophic community ecology models to investigate and understand daily ecological dynamics in the near-surface ocean including impacts of light-driven growth, viral infection, and grazing on Prochlorococcus, the main primary producer in this ecosystem. Model-data fits reveal that integrating top-down processes with light-driven growth can jointly explain diel changes in cyanobacteria, (including infected cells), virus, and grazer abundances. Moreover, direct comparisons of in silico dynamics with in situ observations can be used to partition the relative contributions of viral-induced lysis and grazing to Prochlorococcus mortality. Model-based inferences estimate virus-induced lysis and grazing to contribute < 5% and > 90%, respectively, to overall Prochlorococcus mortality -- providing further support for recent observations that viral-induced lysis is relatively unimportant in shaping Prochlorococcus mortality in surface waters of the NPSG. While our results suggest grazing and viral-lysis explain ≈ 95% of Prochlorococcus mortality, our model-data integration also finds that a modest, but nonetheless statistically significant component of estimated Prochlorococcus mortality (≈ 5% with 95% confidence intervals ranging from less than 1% to 27%) was not attributed to either viral lysis by T4- or T7-like cyanophages or grazing by heterotrophic nanoflagellates. Instead, model-data integration suggests the ecological relevance of other mortality mechanisms in structuring Prochlorococcus populations in the NPSG -- likely by mixotrophic nanoflagellates, but potentially including grazing by other predators, lysis by other cyanophages, particle aggregation, and stress-induced loss mechanisms. Altogether, combining mechanistic multitrophic models with high-resolution measurements provides a route to quantify the balance of bottom-up and top-down forces in the NPSG while identifying the potential for non-canonical factors to shape the structure and function of marine microbial communities.Competing Interest StatementThe authors have declared no competing interest.Footnotes* We have performed major revisions to this paper including a major overhaul of code and methods, choosing to focus our attention on the ECLIP model framework and data-integration via Bayesian parameter inference and analysis. We also provide a more detailed analysis of where models may sit along the grazer specialism-generalism spectrum.* https://doi.org/10.5281/zenodo.7388552

Background Sedentary time is associated with chronic disease and premature mortality. We tested a multilevel workplace intervention with and without sit-stand workstations to reduce sedentary time and lower cardiometabolic risk. Methods Stand and Move at Work was a group (cluster) randomized trial conducted between January 2016 and December 2017 among full-time employees; ≥18 years; and in academic, industry/healthcare, and government worksites in Phoenix, Arizona and Minneapolis/St. Paul, Minnesota, USA. Eligible worksites were randomized to (a) MOVE+ , a multilevel intervention targeting reduction in sedentary time and increases in light physical activity (LPA); or (b) STAND+ , the MOVE+ intervention along with sit-stand workstations to allow employees to sit or stand while working. The primary endpoints were objectively-measured workplace sitting and LPA at 12 months. The secondary endpoint was a clustered cardiometabolic risk score (blood pressure, glucose, insulin, triglycerides, and HDL-cholesterol) at 12 months. Results Worksites ( N  = 24; academic [ n  = 8], industry/healthcare [ n  = 8], and government [ n  = 8] sectors) and employees ( N  = 630; 27 ± 8 per worksite; 45 ± 11 years of age, 74% female) were enrolled. All worksites were retained and 487 participants completed the intervention and provided data for the primary endpoint. The adjusted between arm difference in sitting at 12 months was − 59.2 (CI: − 74.6,-43.8) min per 8 h workday, favoring STAND+ , and in LPA at 12 months was + 2.2 (− 0.9,5.4) min per 8 h workday. Change in the clustered metabolic risk score was small and not statistically significant, but favored STAND+. In an exploratory subgroup of 95 participants with prediabetes or diabetes, the effect sizes were larger and clinically meaningful, all favoring STAND+, including blood glucose, triglycerides, systolic blood pressure, glycated hemoglobin, LDL-cholesterol, body weight, and body fat. Conclusions Multilevel workplace interventions that include the use of sit-stand workstations are effective for large reductions in sitting time over 12 months. Among those with prediabetes or diabetes, clinical improvements in cardiometabolic risk factors and body weight may be realized. Trial registration ClinicalTrials.gov Identifier: NCT02566317 . Registered 2 October 2015, first participant enrolled 11 January 2016.

Although many selection estimates have been published, the environmental factors that cause selection to vary in space and time have rarely been identified. One way to identify these factors is by experimentally manipulating the environment and measuring selection in each treatment. We compiled and analyzed selection estimates from experimental studies. First, we tested whether the effect of manipulating the environment on selection gradients depends on taxon, trait type, or fitness component. We found that the effect of manipulating the environment was larger when selection was measured on life-history traits or via survival. Second, we tested two predictions about the environmental factors that cause variation in selection. We found support for the prediction that variation in selection is more likely to be caused by environmental factors that have a large effect on mean fitness but not for the prediction that variation is more likely to be caused by biotic factors. Third, we compared selection gradients from experimental and observational studies. We found that selection varied more among treatments in experimental studies than among spatial and temporal replicates in observational studies, suggesting that experimental studies can detect relationships between environmental factors and selection that would not be apparent in observational studies.

Australopithecus sediba has been hypothesized to be a close relative of the genus Homo. Here we show that MH1, the type specimen of A. sediba , was not optimized to produce high molar bite force and appears to have been limited in its ability to consume foods that were mechanically challenging to eat. Dental microwear data have previously been interpreted as indicating that A. sediba consumed hard foods, so our findings illustrate that mechanical data are essential if one aims to reconstruct a relatively complete picture of feeding adaptations in extinct hominins. An implication of our study is that the key to understanding the origin of Homo lies in understanding how environmental changes disrupted gracile australopith niches. Resulting selection pressures led to changes in diet and dietary adaption that set the stage for the emergence of our genus. Dietary adaptations of extinct early humans are often inferred from dental microwear data. Here, the authors employ mechanical analyses to show that Australopithecus sediba had limited ability to consume hard foods.