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Demory, D.

Publications and source records attributed to Demory, D..

14 recordsLinked to original sources

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↗

Connecting models, networks and experiments: Revisiting the role of viruses in marine carbon cycling

The marine microbial food web is a key driver of global carbon cycling, mediating the production, consumption and remineralisation of organic matter in the ocean. Within this food web, viruses exert strong top-down control by infecting and lysing both phytoplankton and heterotrophic bacteria. Although virus-induced mortality is recognised as a factor shaping microbial dynamics, accurately quantifying its contribution to carbon cycling remains difficult. A range of approaches have been used to estimate this contribution, notably: (1) dynamical microbial ecosystem models, (2) static carbon flux networks, and (3) direct measurements of virus-induced mortality, such as dilution assays. In this study, we bring these approaches together by formulating them within a common mathematical framework. This enables us to clarify the difference between two notions of lysis percentage in the literature, to compare predictions of previous microbial ecosystem models and flux network reconstructions, and to critically evaluate the theoretical approach of eliminating viruses from the system to explore their effects. Our analysis clarifies how the different approaches capture complementary aspects of the role of marine viruses in carbon cycling across varying spatial and temporal scales.

ecology↗

Genomic analysis of Ostreococcus tauri-infecting viruses reveals a hypervariable region associated with host--virus interactions

While the genus Prasinovirus, known to infect prasinophyte green algae (class Mamiellophyceae), is abundant in the oceans, the genetic mechanisms governing the ecology and (co)evolution of these viruses remain poorly understood. In this study, we sequenced the complete genomes of eighteen viruses infecting the cosmopolitan unicellular green alga Ostreococcus tauri (OtVs) and one specific to Micromonas commoda (McV-20T). Of these viruses, twelve were previously isolated from the coastal Mediterranean Sea and seven were newly isolated from two different geographical locations (i.e., the South Pacific Gyre and the North Sea). Phylogenetic analysis classified these viruses as new members of the Prasinovirus genus and defined three distinct OtV clades: designated OtV-type 1, OtV-type 2a and OtV-type 2b. The OtV-type 1 includes three new viruses isolated from the Pacific Ocean and the previously sequenced genome OtV6. The OtV-type 1 form a large cluster within the Micromonas-infecting virus clade, sharing five unique homologous genes with all Micromonas viruses. In addition, genetic features of OtV-type 1, including a higher number of CDSs ([~]260) and lower GC content ([~]41%), were more closely allied to Micromonas viruses than to those of OtVs, suggesting an alternative host or a recent host switch from Micromonas to O. tauri. By analyzing the OtV genomes, we found a faster-evolving central hypervariable region (HVR), where the OtV-type 2b displayed the largest region, i.e., three times longer than other OtVs. This region encodes genes mainly associated with host cell recognition and attachment and under strong selective pressure (positive and negative). Notably, most viruses associated with OtV-type 2b showed the broadest host range. Infection dynamics between the hosts and the viruses appeared highly specific to host-virus pairs, suggesting complex interactions in the Ostreococcus-prasinovirus system. Finally, by observing viral lysates with electron microscopy, we observed novel morphologies never described for these viruses. Overall, this study provides new insights into the genetic diversity of prasinoviruses and describes for the first time a viral plasticity that might be strongly shaped by antagonistic coevolution with their hosts.

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↗

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↗

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↗

Emergence and maintenance of stable coexistence during a long-term multicellular evolution experiment

The evolution of multicellular life spurred evolutionary radiations, fundamentally changing many of Earths ecosystems. Yet little is known about how early steps in the evolution of multicellularity transform eco-evolutionary dynamics, e.g., via niche expansion processes that may facilitate coexistence. Using long-term experimental evolution in the snowflake yeast model system, we show that the evolution of multicellularity drove niche partitioning and the adaptive divergence of two distinct, specialized lineages from a single multicellular ancestor. Over 715 daily transfers, snowflake yeast were subject to selection for rapid growth in rich media, followed by selection favoring larger group size. Both small and large cluster-forming lineages evolved from a monomorphic ancestor, coexisting for over ~4,300 generations. These small and large sized snowflake yeast lineages specialized on divergent aspects of a trade-off between growth rate and survival, mirroring predictions from ecological theory. Through modeling and experimentation, we demonstrate that coexistence is maintained by a trade-off between organismal size and competitiveness for dissolved oxygen. Taken together, this work shows how the evolution of a new level of biological individuality can rapidly drive adaptive diversification and the expansion of a nascent multicellular niche, one of the most historically-impactful emergent properties of this evolutionary transition.

evolutionary biology↗

Global phylogeography of marine Synechococcus in coastal areas reveals strikingly different communities than in the open ocean

Marine Synechococcus comprise a numerically and ecologically prominent phytoplankton group, playing a major role in both carbon cycling and trophic networks in all oceanic regions except in the polar oceans. Despite their high abundance in coastal areas, our knowledge of Synechococcus communities in these environments is based on only a few local studies. Here, we use the global metagenome dataset of the Ocean Sampling Day (June 21st 2014) to get a snapshot of the taxonomic composition of coastal Synechococcus communities worldwide, by recruitment on a reference database of 141 picocyanobacterial genomes, representative of the whole Prochlorococcus, Synechococcus and Cyanobium diversity. This allowed us to unravel drastic community shifts over small to medium scale gradients of environmental factors, in particular along European coasts. The combined analysis of the phylogeography of natural populations and the thermophysiological characterization of eight strains, representative of the four major Synechococcus lineages (clades I to IV), also brought novel insights about the differential niche partitioning of clades I and IV, which most often co-dominate the Synechococcus community in cold and temperate coastal areas. Altogether, this study tackles the main differences between open-ocean and coastal communities worldwide.

microbiology↗

Diel population dynamics and mortality of Prochlorococcus in the North Pacific Subtropical Gyre

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 function as the primary top-down factor despite high standing viral particle densities while identifying the potential for light-dependent viral traits and non-canonical loss factors to shape the structure and function of marine microbial communities.

ecology↗

A thermal trade-off between viral production and degradation drives phytoplankton-virus population dynamics

Marine viruses interact with their microbial hosts in dynamic environments shaped by variations in abiotic factors, including temperature. However, the impacts of temperature on viral infection of phytoplankton are not well understood. Here we coupled mathematical modeling with experimental datasets to explore the effect of temperature on three Micromonas-prasinovirus pairs. Our model shows the negative consequences of high temperatures on infection and suggests a temperature-dependent threshold between viral production and degradation. Modeling long-term dynamics in environments with different average temperatures revealed the potential for long-term host-virus coexistence, epidemic free, or habitat loss states. Hence, we generalized our model to global sea surface temperature of present and future seas and show that climate change may influence virus-host dynamics differently depending on the virus-host pair. Our study suggests that temperature-dependent changes in the infectivity of virus particles may lead to shifts in virus-host habitats in warmer oceans, analogous to projected changes in the habitats of macro- and micro-organisms.

ecology↗

Linking light-dependent life history traits with population dynamics for Prochlorococcus and cyanophage

Prochlorococcus grow in diurnal rhythms driven by diel cycles. Their ecology depends on light, nutrients, and top-down mortality processes including lysis by viruses. Cyanophage, viruses that infect cyanobacteria, are also impacted by light. For example, extracellular viability and intra-cell infection kinetics of some cyanophage vary between light and dark conditions. Nonetheless, it remains unclear if light-dependent viral life history traits scale-up to influence population-level dynamics. Here we examined the impact of diel-forcing on both cellular- and population-scale dynamics in multiple Prochlorococcus-phage systems. To do so, we developed a light-driven population model including both cellular growth and viral infection dynamics. We then tested the model against measurements of experimental infection dynamics with diel forcing to examine the extent to which population level changes in both viral and host abundances could be explained by light-dependent life history traits. Model-data integration reveals that light-dependent adsorption can improve fits to population dynamics for some virus-host pairs. However, light-dependent variation alone does not fully explain realized host and virus population dynamics. Instead, we show evidence of a previously unrecognized lysis saturation at relatively high virus to cell ratios. Altogether, our study represents a quantitative approach to integrate mechanistic models to reconcile Prochlorococcus-virus dynamics spanning cellular to population scales.

microbiology↗