bioRxiv Science⌕ Search

Biology subjects

Weitz, J. S.

Publications and source records attributed to Weitz, J. S..

At least 19 recordsLinked to original sources

Slower-than-exponential viral decay is prevalent and can reshape virus-microbe dynamics

Viral population dynamics are shaped by production and loss. For viruses of microbes, high standing levels of viral abundances are interpreted as evidence of high rates of viral-induced cellular loss and viral production, followed by rapid extracellular viral decay. Here we reassess assumptions of rapid extracellular decay in 17 curated datasets, finding that biphasic decay either fits better or is statistically indistinguishable from exponential decay in approximately half the datasets. In addition to intrinsic heterogeneity in decay rates, biphasic decay at population scales can arise generically through aggregation mechanisms, where single virions decay and viral aggregates are protected. Integrating aggregation-induced biphasic decay into a virus-host model reveals that accounting for aggregation can recapitulate joint observations of high virion abundances and low infection prevalence, without assuming significant levels of uniformly inefficient infection. Together, our results suggest that durable extracellular virion persistence is environmentally relevant in shaping virus-microbe population dynamics.

ecology↗

Implicit representation of viruses fails to capture impacts of virus-induced mortality in global marine ecosystem models

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 PointsO_LIGlobal model reveals significant spatial heterogeneity arising from explicit, rather than implicit, representation of viruses C_LIO_LIImplicit representation of viral dynamics fails to capture the potential for viruses to terminate phytoplankton blooms C_LIO_LIBiogeochemical models require explicit representation of viruses to adequately simulate their effect on marine systems C_LI

microbiology↗

Virus-grazer interplay enhances virus production, particle aggregation, and trophic efficiency during infection of Prochlorococcus

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. SignificanceViruses 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.

microbiology↗

Viral impacts on plankton standing stocks, primary productivity, and biogeochemistry in a model ocean

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.

ecology↗

Sub-daily Bermuda Atlantic Time Series virus sampling reveals taxonomy, host, and functional differences at the population, but not community level

Ocean microbes contribute to biogeochemical cycles and ecosystem function, but they do so under top-down pressure imposed by viruses. While viruses are increasingly understood spatially and beginning to be incorporated into predictive modeling, high-frequency ocean virus dynamics remain understudied due to methodological challenges. Here we sampled stratified Bermuda Atlantic Time Series (BATS) waters for 112 hours at sub-daily 4-(surface) or 12-(deep chlorophyll maximum) hour intervals, purified viral particles from these samples, sequenced their metagenomes, and used the resulting data to characterize high-frequency virus community dynamics. Aggregated community diversity metrics changed with depth, but were not statistically significant temporally at a fixed location. However, finer-scale population-level analyses revealed both depth and temporal change, including physicochemical depth-driven differences and, in surface waters, thousands of viral populations that exhibited statistically significant diel rhythms. Statistical analyses revealed three main archetypes of temporal dynamics that themselves differed in abundance patterns, host predictions, viral taxonomy, and gene functions. Among these, highlights include viruses resembling an archetype with a night peaking pattern in activity that include an over-representation of viruses that putatively infect Prochlorococcus, a phototrophic cyanobacteria. Together, these efforts provide baseline community-and population-scale short-time-frame observations relevant to future climate state modeling.

microbiology↗

Prophage induction states drive structural and synergistic outcomes in marine bacterial biofilms

Microbes commonly live in biofilms, dense spatially structured assemblages where temperate phages can influence interactions amongst closely related strains. Yet, how these phage-host interactions impact biofilm architecture and ecological dynamics remains poorly understood, particularly in situations where antagonistic strains coexist in structured communities. In the marine Roseobacteraceae Sulfitobacter pontiacus, two genetically similar heteroimmune prophages, (termed A and D) establish lysogeny in their host. Depending on the host plasmid genotype, prophages are fixed in either high or low induction states, which consequently shape both biofilm structure and competitive outcomes. Using confocal scanning laser microscopy of fluorescently labeled lysogens, we investigated how prophage induction and phage genotype of phage-host coalitions influence monoculture and co-culture (competitive) S. pontiacus biofilms grown at a fluid-solid interface. Compared to their low induction counterparts, high-induction strains formed thicker and more voluminous monoculture biofilms, which primarily result from vertical protrusions arising from a basal monolayer. In co-culture experiments - mixing strains with reciprocal prophage genotypes that can mutually kill each other through phage-mediated allelopathy - we observed unexpected coexistence and synergistic biofilm enhancement rather than competitive exclusion. Reactive oxygen species (ROS) levels were significantly higher in co-cultures than monocultures and correlated with local cell density, suggesting that phage-mediated interactions generate hotspots of oxidative stress, which is expected to further promote prophage induction, creating a positive feedback loop that amplifies cell lysis and release of matrix components. These results suggest temperate phages can paradoxically stabilize and promote biofilm growth via mechanisms that combine antagonistic killing with cooperative matrix production, revealing how phage-mediated interactions can shape microbial community architecture in spatially structured environments. IMPORTANCEBacterial biofilms are ubiquitous in natural environments, yet understanding of how temperate bacteriophages shape biofilm development and microbial community dynamics remains limited. Here, we demonstrate that prophage induction state simultaneously drives antagonistic killing and cooperative biofilm enhancement in spatially structured microbial communities. Using Sulfitobacter pontiacus and its infecting temperate phages as a model system, we reveal that reciprocally antagonistic host-phage pairs, which can kill each other through phage-mediated allelopathy, form more robust biofilms when grown together rather than separately. These findings challenge traditional views of competition in dense microbial systems, highlighting the complex, multi-faceted roles that temperate phages play in microbial communities. Additionally, we propose that oxidative stress creates positive feedback loops that amplify prophage induction, promoting coexistence of host-phage pairs rather than driving competitive exclusion. These insights have broad implications for understanding microbial community assembly, maintenance of genetic diversity in biofilms, and evolutionary dynamics of host-phage interactions in structured environments.

microbiology↗

Phase separation and coexistence in spatial coordination games between microbes

Dense, microbial communities are shaped by local interactions between cells. Both the nature of interactions, spanning antagonistic to cooperative, and the strength of interactions vary between and across microbial species and strains. These local interactions can influence the emergence and maintenance of microbial diversity. However, it remains challenging to link features of local interactions with spatially mediated coexistence dynamics given the significant variation in the microscopic mechanisms involved in cell-to-cell feedback. Here, we explore how microbial interactions over a broad range of ecological contexts spanning antagonism to cooperation can enable coexistence as spatially explicit domains emerge. To do so, we introduce and analyze a family of stochastic coordination games, where individuals do better when playing (i.e., interacting) with individuals of the same type than when playing with individuals of a different type. Using this game-theoretic framework, we show that the population dynamics for coordination games is governed by a double-well shaped interaction potential. We find that in a spatial setting this double-well potential induces phase separation, facilitating coexistence. Moreover, we show that for microbes engaged in symmetric coordination games, phase separation takes on a universal scaling that follows Model A coarsening, consistent with prior experimental observations for Vibrio cholerae mutual killers. Finally, we derive a PDE equivalent of the spatial stochastic game, confirming both the double-well nature of spatial coordination games and the universality of phase separation. Altogether, this work extends prior findings on the link between microbial interactions and population structure and suggests generic mechanisms embedded in local interactions that can enable coexistence.

microbiology↗

Coexistence of Photosynthetic Marine Microorganisms, Viruses, and Grazers: Toward Integration in Ocean Ecosystem Models

Photosynthetic microorganisms are responsible for primary production at the base of the marine food web that impacts ocean biogeochemistry and ecological interactions. The growth of these microorganisms is balanced by mortality processes, including top-down losses from zooplankton grazing and infection and lysis by viruses. Multiple types of grazers and viruses often coexist despite apparent competition for the same (or similar) microorganisms. Here, we develop a community model of photosynthetic microorganisms, grazers, and viruses that accounts for molar cell and virion elemental quotas suitable for incorporation into ocean ecosystem models. Our aim is to investigate mechanisms that enable coexistence of a virus and a grazer with a single phytoplankton type. To do so, we evaluate the extent to which coexistence is facilitated by: (i) infected phytoplankton, potentially subject to non-preferential intraguild predation, where grazers feed on virally infected microorganisms; (ii) heterogeneity in susceptibility to infection, where microorganisms vary in their resistance to the virus either intracellularly or extracellularly; and (iii) the inclusion of higher-order mortality terms for the predators. We find evidence for a trade-off between the virus latent period and virulence in facilitating a coexistence regime. The inclusion of an explicit latent period can generate oscillations of all populations that facilitate coexistence by reducing the growth rate of the free virus, or lead to system collapse when oscillations become too large. Heterogeneity in phage susceptibility promotes coexistence through resource partitioning between the predators, while higher-order mortality terms widen the coexistence regime by stabilizing the system. We observe strong sensitivity of model outcomes to viral life history traits, including shifts in infected cell percentages and the balance between virally and zooplankton-induced mortality. Finally, taking advantage of algebraic calculation of model equilibria, we identify life history trait parameter combinations that yield realistic ecological properties in simplified oligotrophic and mesotrophic epipelagic environments. Importantly, our ecological models suggest that ongoing efforts to embed virus dynamics in large-scale ocean ecosystem models should likely include phytoplankton types that are moderately to strongly resistant to viral infection and lysis.

ecology↗

Emergent higher-order interactions enable coexistence in phage-bacteria community dynamics

Diverse phage-bacteria communities coexist at high densities in environmental, agricultural, and human-associated microbiomes. Phage-bacteria coexistence is often attributed to coevolutionary processes mediated by complex, pairwise infection networks. Here, using in vitro experiments and mathematical models, we explore how higher-order interactions function as a complementary, ecological feedback mechanism to stabilize phage-bacteria communities. To do so, we examine an environmentally-derived, synthetic phage-bacteria community comprised of five marine heterotrophic bacteria (Cellulophaga baltica and Pseudoalteromonas strains) and five associated phage. We used Bayesian inference to reconstruct free phage production in one-step growth experiments and then forecasted pairwise phage-bacteria community dynamics over multiple infection cycles. In contrast to model predictions of rapid bacterial population collapse, each bacterial strain persisted in the community. We hypothesized and then experimentally validated the relevance of infection attenuation at relatively high viral densities. We extended models into a community context, corroborating complex coexistence of all phage and bacteria. Life history traits inferred in community fits often differed from those inferred in a pairwise context, implicating higher-order interactions as an additional, ecological stabilization mechanism. Follow-up experiments confirm that phage traits (including burst size) can shift when infecting single vs. multiple strains. More broadly, these findings suggest that complex community coexistence of phage and bacteria may be more common than anticipated when including feedback mechanisms outside of the growth-dominated regimes of fitted pairwise models that do not reflect the full scope of ecologically relevant contexts.

ecology↗

Stable coexistence and transport of lytic phage infections with migrating bacterial hosts

Bacteriophages (phages), viruses that exclusively infect bacteria, coexist with their bacterial hosts across diverse environments at densities exceeding 107 ml-1 in marine surface waters, 108 ml-1 in soils, and 109 ml-1 in the human gut1-6. In contrast, phage lysis of bacteria populations within well-mixed in vitro environments select for the emergence of phage-resistant bacterial mutants7, which in turn select for host-range expansion phage mutants8,9 and, typically, the collapse of phage populations altogether10,11. This gap in outcome raises a question: what enables long-term phage-bacteria coexistence? Here, we show how interactions in space can facilitate stable coexistence and long-range transport of virulent phage along with migrating bacteria. Combining theory, simulation, and experiments across multiple phage-bacteria systems, we reveal a chemotaxis-driven mechanism that robustly stabilizes coexistence and dispersal of virulent phages with migrating hosts. These findings suggest the ecological relevance of spatial interaction mechanisms that reinforce stability between antagonistic partners in the absence of perpetual cycles of defense and counter-defense, which may be broadly applicable across phage-bacteria systems.

ecology↗

Viral community diversity in the rhizosphere of the foundation salt marsh plant Spartina alterniflora

Viruses of microorganisms impact microbial population dynamics, community structure, nutrient cycling, gene transfer, and genomic innovation. In wetlands, root-associated microbial communities mediate key biogeochemical processes important for plants involved in ecosystem maintenance. Nonetheless, the presence and role of microbial viruses in salt marshes remains poorly understood. In this study, we analyzed 24 metagenomes retrieved from the root zone of Spartina alterniflora, a foundation plant in salt marshes of the eastern and Gulf coasts of the U.S. The samples span three plant compartments--bulk sediment, rhizosphere, and root--and two cordgrass plant phenotypes: short and tall. We observed differentiation between phenotypes and increased similarity in viral communities between the root and rhizosphere, indicating that plant compartment and phenotype shape viral community composition. The majority of viral populations characterized are novel at the genus level, with a subset predicted to target microorganisms known to carry out key biogeochemical functions. The findings provide a holistic assessment of plant-associated viral diversity and community composition as well as identifying potential targets for exploring viral modulation of microbially-mediated ecosystem functioning in intertidal wetlands. ImportanceSalt marshes are vital coastal ecosystems. Microbes in these environments drive nutrient cycling and support plant health, with Spartina alterniflora serving as a foundation species. This study explores viral communities associated with S. alterniflora, revealing how plant compartment and phenotype shape viral composition. The discovery of numerous novel viruses, some potentially influencing microbes involved in key biogeochemical processes, highlights their ecological significance. Given the increasing pressures on coastal ecosystems, understanding virus-microbe-plant interactions is essential for predicting and managing ecosystem responses to environmental change.

genomics↗

Inferring single-cell heterogeneity of bacteriophage life-history traits from population-scale dynamics

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 Syn9s 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.

microbiology↗

Seasonal Enhancement of the Viral Shunt Catalyzes a Subsurface Oxygen Maximum in the Sargasso Sea

Subsurface oxygen maxima (SOMs) occur directly beneath the mixed layer of stratified water columns across oligotrophic open ocean basins. SOMs occur seasonally and are hypothesized to result from elevated microbial net primary productivity (NPP). Here, we set out to identify mechanistic drivers of the SOM near the Bermuda Atlantic Time Series (BATS) site in the Sargasso Sea in October 2019. Coupled time-series analysis of metatranscriptomics, flow cytometry, and family-specific cyanophage quantification revealed elevated Prochlorococcus abundances, cyanophage abundances, and cyanophage-specific transcriptional activity in the SOM. These findings spurred us to analyze historical oxygen saturation profiles at BATS - identifying a repeated, seasonal cycle in SOM emergence associated with elevated virus-like particles and Prochlorococcus numbers. Returning to the 2019 study site, we found that transcriptional markers for increased dissolved organic matter uptake by copiotrophic bacteria were enriched in the SOM, consistent with enhanced catabolic activity due to the viral shunt. In addition, Prochlorococcus exhibited enrichment in ammonium transport transcripts at the SOM, consistent with increased responsiveness to remineralization activity by heterotrophs. Altogether, these findings suggest that enhanced viral lysis leads to locally elevated nutrient recycling and oxygen production, further reinforcing hypotheses that viruses may play a critical role in the emergence of SOMs in the oligotrophic ocean.

ecology↗

Temperature-driven biogeography of marine giant viruses infecting the picoeukaryote Micromonas

Climate shapes the biogeography of microbial and viral communities in the ocean. Among abiotic factors, temperature is one of the main drivers of microbial community distribution. However, we lack knowledge on how temperature shapes the life history traits, population dynamics, and the biogeography of marine viruses. This study integrates mathematical modeling with in situ observations to investigate the temperature-driven biogeography of marine viruses. We focused on prasinoviruses, a group of giant viruses that infect the picoeukaryote Micromonas, a widespread phytoplankton with thermotypes adapted from poles to tropics. Analyzing the Tara Oceans and Polar Circle databases, we found that temperature is the primary determinant of Micromonas virus (MicV) distribution in the surface ocean. Phylogenetic reconstruction of MicV-s revealed that these viruses form several groups with cryophile or cryo-mesophile preferences. We applied a mechanistic model to describe temperature-driven population dynamics, allowing us to predict the global presence and absence of MicV-s. Lysis and infection emerged as reliable predictors of MicV distribution, indicating that temperature-driven cellular mechanisms significantly shape viral community structure and distribution. This study provides new insights into the role of temperature in regulating viral populations, emphasizing the importance of integrating modeling with observations to understand marine viral ecology.

ecology↗

Multi-strain phage induced clearance of bacterial infections

Bacteriophage (or phage - viruses that infect and kill bacteria) are increasingly considered as a therapeutic alternative to treat antibiotic-resistant bacterial infections. However, bacteria can evolve resistance to phage, presenting a significant challenge to the near- and long-term success of phage therapeutics. Application of mixtures of multiple phage (i.e., cocktails) have been proposed to limit the emergence of phage-resistant bacterial mutants that could lead to therapeutic failure. Here, we combine theory and computational models of in vivo phage therapy to study the efficacy of a phage cocktail, composed of two complementary phages motivated by the example of Pseudomonas aeruginosa facing two phages that exploit different surface receptors, LUZ19v and PAK P1. As confirmed in a Luria-Delbruck fluctuation test, this motivating example serves as a model for instances where bacteria are extremely unlikely to develop simultaneous resistance mutations against both phages. We then quantify therapeutic outcomes given single- or double-phage treatment models, as a function of phage traits and host immune strength. Building upon prior work showing monophage therapy efficacy in immunocompetent hosts, here we show that phage cocktails comprised of phage targeting independent bacterial receptors can improve treatment outcome in immunocompromised hosts and reduce the chance that pathogens simultaneously evolve resistance against phage combinations. The finding of phage cocktail efficacy is qualitatively robust to differences in virus-bacteria interactions and host immune dynamics. Altogether, the combined use of theory and computational analysis highlights the influence of viral life history traits and receptor complementarity when designing and deploying phage cocktails in immunocompetent and immunocompromised hosts.

microbiology↗

Eco-evolutionary dynamics of temperate phages in periodic environments

Bacteriophage (viruses that exclusively infect bacteria) exhibit a continuum of infection mechanisms, including lysis and lysogeny in interactions with bacterial hosts. Recent work has demonstrated the near-term advantages of lysogeny over lysis in conditions of low host availability. Hence, temperate phage which can switch between lytic and lysogenic strategies -- both stochastically and responsively -- are hypothesized to have an evolutionary advantage in a broad range of conditions. To examine generalized drivers of viral strategies over the near- and long-term, we explore the eco-evolutionary dynamics of temperate viruses in periodic environments with varying levels of host availability and viral mortality. We use a nonlinear system of ordinary differential equation to simulate periodically-forced dynamics that separate a within-epoch phase and a between-epoch phase, in which a (potentially unequal) fraction of virus particles and lysogens survive. Using this ecological model and invasion analysis, we show and quantify how conflicts can arise between strategies in the near-term that may favor lysis and strategies in the long-term that may favor lysogeny. In doing so, we identify a wide range of conditions in which temperate strategies can outperform obligately lytic or lysogenic strategies. Finally, we demonstrate that temperate strategies can mitigate against the potential local extinction of viruses in stochastically fluctuating environments, providing further evidence of the eco-evolutionary benefits of being temperate.

ecology↗

Episomal virus maintenance enables bacterial population recovery from infection and virus-bacterial coexistence

Hypersaline environments harbor the highest concentrations of virus-like particles (VLPs) reported for aquatic ecosystems. The substantial densities of both microbial populations and VLPs challenge traditional explanations of top-down control exerted by viruses. At close to saturation salinities, prokaryotic populations are dominated by Archaea and the bacterial clade Salinibacter. In this work we examine the episomal maintenance of a virus within a Salinibacter ruber host. We found that infected cultures of Sal. ruber M1 developed a population-level resistance and underwent systematic and reproducible recovery post infection that was counter-intuitively dependent on the multiplicity of infection (MOI), where higher MOI led to better host outcomes. Furthermore, we developed a nonlinear population dynamics model that successfully reproduced the qualitative features of the recovery. This suggests that the maintenance of the virus episomally, often referred to as pseudolysogeny, and lysis inhibition allow for host-virus co-existence under high MOI infections. Our results emphasize the ecological importance of exploring a spectrum of viral infection strategies beyond the conventional binary of lysis or lysogeny.

microbiology↗

Accounting for Cellular-Level Variation in Lysis: Implications for Virus-Host Dynamics

Viral impacts on microbial populations depend on interaction phenotypes - including viral traits spanning adsorption rate, latent period, and burst size. The latent period is a key viral trait in lytic infections. Defined as the time from viral adsorption to viral progeny release, the latent period of bacteriophage is conventionally inferred via one-step growth curves in which the accumulation of free virus is measured over time in a population of infected cells. Developed more than 80 years ago, one-step growth curves do not account for cellular-level variability in the timing of lysis, potentially biasing inference of viral traits. Here, we use nonlinear dynamical models to understand how individual-level variation of the latent period impacts virus-host dynamics. Our modeling approach shows that inference of latent period via one-step growth curves is systematically biased - generating estimates of shorter latent periods than the underlying population-level mean. The bias arises because variability in lysis timing at the cellular level leads to a fraction of early burst events which are interpreted, artefactually, as an earlier mean time of viral release. We develop a computational framework to estimate latent period variability from joint measurements of host and free virus populations. Our computational framework recovers both the mean and variance of the latent period within simulated infections including realistic measurement noise. This work suggests that reframing the latent period as a distribution to account for variability in the population will improve the study of viral traits and their role in shaping microbial populations. ImportanceQuantifying viral traits - including the adsorption rate, burst size, and latent period - is critical to characterize viral infection dynamics and to develop predictive models of viral impacts across scales from cells to ecosystems. Here, we revisit the gold standard of viral trait estimation - the one-step growth curve - to assess the extent to which assumptions at the core of viral infection dynamics lead to ongoing and systematic biases in inferences of viral traits. We show that latent period estimates obtained via one-step growth curves systematically under-estimate the mean latent period and, in turn, over-estimate the rate of viral killing at population scales. By explicitly incorporating trait variability into a dynamical inference framework that leverages both virus and host time series we provide a practical route to improve estimates of the mean and variance of viral traits across diverse virus-microbe systems.

ecology↗