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Beckett, S. J.

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

11 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↗

Molecular resources for the stored grain Cryptolestes cryptic pest species (Coleoptera: Laemophloeidae)

Recent research activities relating to evolutionary genetics and molecular characterisation of the stored grain Cryptolestes (Ganglbauer) beetle pest species have revealed gaps in public DNA databases, and resulted in molecular diagnostic inconsistencies. This study reports on characterisation of the mitochondrial DNA cytochrome oxidase I (mtCOI) gene from specimens detected during biosecurity inspections at Australias border, and surveys of publicly available mtCOI gene sequences, for re-assessment of Cryptolestes species status. The results enabled clarification of a new putative C. sp. WTT-2016 species, and supported the close evolutionary relationships between C. ferrugineus (Stephens)/C. pusilloides (Steel and Howe), and between C. pusillus (Schonherr) and the previously identified C. sp. WTT-2013 cryptic species. Widespread confusion between C. ferrugineus, C. pusiolloides, C. pusillus and the two putative novel C. sp. WTT-2013 and C. sp. WTT-2016, highlighted the taxonomic challenge surrounding this beetle genus, while inter-specific genetic distances between C. spartii (Curtis)/C. corticinus (Reitter) suggested they belonged to the same species. Assembled and annotated mitochondrial DNA genomes (mitogenomes) of six Cryptolestes species via high throughput sequencing identified assembly errors associated with published mitogenomes of C. ferrugineus and C. turcicus (Grouvelle), and misidentification of C. pusillus. Based on re-evaluation of intra- and inter-specific genetic distances and congruence from phylogenetic inferences, we proposed a Cryptolestes species genetic gap at approximately 5% that could help with defining species boundaries. By reconciling these molecular incongruences, this study will contribute to improving agricultural biosecurity preparedness associated with the economically important Cryptolestes flat grain beetle species.

evolutionary biology↗

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↗

Deciphering the dynamics of Cyanobacteria-Phage in a natural lake: Insights from a decade-long investigation

Phages - viruses that infect bacteria - are often seen as key players in bacterial community dynamics and the ecosystem services those communities support. However, much of our understanding of phage-bacteria interactions comes from in vitro studies, which provide limited insights into how these interactions occur in natural environments. In this study, we used cyanobacterial blooms as a model microbial community to evaluate the potential role of phages in driving cyanobacterial populations. These blooms are characterized by massive and usually rapid accumulation of cyanobacterial biomass and occur worldwide, threatening aquatic systems. The frequency and intensity of cyanobacterial blooms are increasing over time, likely due to human activities, and, until now, the role of predators like phages has remained unclear. We used a deep amplicon sequencing approach targeting the g20 capsid gene to profile the cyanophage community in eutrophic Lake Champlain over time, comparing their dynamics and diversity with bacterial communities and examining their associations. We evaluated whether phages simply followed bacterial dynamics, with limited impact on bacterial composition, or instead whether they played an active role in drving bacterial community structure. We found that phages exhibited similar dynamics to their potential bacterial hosts and shared environmental niches. However, we also observed strong differences specific to the phage community, such as inter-annual variation and an increase in Shannon diversity over time. Phage-bacteria and phage-cyanobacteria co-variance uncovered potential interactions that resulted in strongly modular networks. However, while the network structure remained modular, the composition of the modules differed significantly between environmental and temporal conditions. Lastly, viral phylogeny partially explained phage-bacteria co-variance, but only for a small proportion of bacterial ASVs. Our results indicate that phage-bacterial interactions are partly genetically structured and vary within modules across environmental conditions.

ecology↗

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↗

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↗

Community-scale Synchronization and Temporal Partitioning of Gene Expression, Metabolism, and Lipid Biosynthesis in Oligotrophic Ocean Surface Waters

Sunlight drives daily rhythms of photosynthesis, growth, and division of photoautotrophs throughout the surface oceans. However, the cascading impacts of oscillatory light input on diverse microbial communities and community-scale metabolism remains unclear. Here we use an unsupervised machine learning approach to show that a small number of diel archetypes can explain pervasive periodic dynamics amongst more than 65,000 distinct time series, including transcriptional activity, macromolecules, lipids, and metabolites from the North Pacific Subtropical Gyre. Overall, we find evidence for synchronous timing of carbon-cycle gene expression that underlie daily oscillations in the concentrations of particulate organic carbon. In contrast, we find evidence of asynchronous timing in gene transcription related to nitrogen metabolism and related metabolic processes consistent with temporal niche partitioning amongst microorganisms in the bacterial and eukaryotic domains.

ecology↗

The effect of strain level diversity on robust inference of virus-induced mortality

Infection and lysis of phytoplankton by viruses affects population dynamics and nutrient cycles within oceanic microbial communities. However, estimating the quantitative rates of viral-induced lysis remains challenging in situ. The modified dilution method is the most commonly utilised empirical approach to estimate virus-induced killing rates of phytoplankton. The lysis rate estimates of the modified dilution method are based on models of virus-host interactions involving only a single virus and a single host population. Here, using modelling approaches, we examine the robustness of the modified dilution method in multi-strain, complex communities. We assume that strains differ in their life history traits, including growth rates (of hosts) and lysis rates (by viruses). We show that trait differences affect resulting experimental dynamics such that lysis rates measured using the modified dilution method may be driven by the fastest replicating strains; which are not necessarily the most abundant in situ. We discuss the implications of using the modified dilution method and alternative dilution-based approaches for estimating viral-induced lysis rates in marine microbial communities.

microbiology↗