Biology subjects

Lindell, D.

Publications and source records attributed to Lindell, D..

12 recordsLinked to original sources

bioRxiv2026

Defining traits of low-light adapted Prochlorococcus inhabiting surface waters of the Equatorial Pacific Ocean

A diverse array of photosynthetic phytoplankton drives primary production in equatorial surface waters. Among these, the cyanobacterium Prochlorococcus is an important contributor to net primary production in these typically iron-limited, high-nutrient and low-chlorophyll (HNLC) regions. Here, we explore the diversity of these organisms, in part, through targeted enrichment of Prochlorococcus cells using field-based high-speed cell sorting techniques. We demonstrate that the genomes of Prochlorococcus belonging to the low-light adapted LLI clade, and isolated from the surface of the Equatorial Pacific Ocean, are depleted in functions related to the assimilation of urea, nitrite, and amino acids. These are the first examples of LLI Prochlorococcus that have lost the ability to use nitrite, a trait considered to be a core feature of this clade. All new equatorial cultures of LLI Prochlorococcus appear to use a distinct isoform of protoporphyrinogen IX oxidase (HemG), for the biosynthesis of a chlorophyll precursor, that does not require the use of iron-containing heme. In contrast, the heme-dependent HemJ isoform is typically used by Prochlorococcus found outside equatorial HNLC waters. Together, these findings suggest that low-light adapted Prochlorococcus in the equatorial ocean possess accessory gene content that reflects adaptation to the generally iron-limited but nitrogen-replete conditions of surface waters.

microbiology↗

bioRxiv2026

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↗

bioRxiv2026

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↗

bioRxiv2026

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↗

bioRxiv2025

A functional cyanophage thioredoxin increases competitive phage fitness

Viruses carry many homologs of cellular genes as well as small genes of unknown function, often called viral dark matter. One cellular-like gene present in viruses is the redox protein thioredoxin, found in all domains of cellular life. However, the functional relevance and evolutionary benefit of viral-encoded thioredoxins, and small genes of unknown function, remain unclear. Both types of genes are present in marine cyanophages, viruses that infect the globally important marine cyanobacteria. In the T7-like cyanophage, Syn5, the phage thioredoxin overlaps with a small gene of unknown function that we named cve for cyanophage virulence enhancer. While thioredoxin genes are common across a wide variety of viruses infecting diverse host types, we found that cve is restricted to cyanophages. Genetic inactivation of thioredoxin and cve in the Syn5 cyanophage revealed that thioredoxin enhanced phage fitness, increasing phage genome replication and progeny production. Furthermore, redox active Syn5 thioredoxin negatively impacted host growth, indicating that its activity is detrimental to host metabolism. The cve gene increased phage virulence yet reduced phage burst size, and is thus a double-edged sword. Despite this trade-off, cve significantly enhanced overall phage fitness emphasizing the importance of virulence for viral fitness. Our findings indicate that viral-encoded thioredoxin and cve genes differentially alter infection properties to provide an evolutionary advantage to the Syn5 phage. They further reveal the function of a small, cyanophage-specific gene of unknown function, unveiling the first known host-type-specific virulence enhancer in viruses.

microbiology↗

bioRxiv2025

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↗

bioRxiv2025

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↗

bioRxiv2024

Oceanic photosynthesis is directly affected by cyanophage NblA proteins

Marine picocyanobacteria are abundant photosynthetic organisms of global importance. They coexist in the ocean with cyanophages, viruses that infect cyanobacteria. Cyanophages carry many auxiliary metabolic genes acquired from their hosts that are thought to redirect host metabolism for the phages benefit1-5. One such gene is nblA which is present in multiple cyanophage families2,6-8. Under nutrient deprivation the cyanobacterial NblA is responsible for inducing proteolytic degradation of the phycobilisome9-11, the large cyanobacterial photosynthetic light harvesting complex. This increases the pool of amino acids available for essential tasks11, serving as a survival mechanism12. Ectopic expression of different cyanophage nblA genes results in host pigment protein degradation9,6. However, the benefit of the cyanophage-encoded NblA for the cyanophage and the broader impact on the host are unknown. Here, using a recently developed genetic manipulation system for marine cyanophages14, we reveal that cyanophage NblA significantly accelerates the cyanophage infection cycle, directs degradation of the host phycobilisome and other proteins and reduces host photosynthetic light harvesting efficiency. Metagenomic analysis revealed that cyanophages carrying nblA are widespread in the oceans and compose 35% and 65% of oceanic T7-like cyanophages in the surface and deep photic zones, respectively. Our results show a large benefit of the nblA gene to the cyanophage while exerting a negative effect on the host photosynthetic apparatus and host photosynthesis. These findings suggest that cyanophage nblA has an adverse global impact on light harvesting by oceanic picocyanobacteria.

microbiology↗

bioRxiv2024

Adaptive loss of tRNA gene expression leads to phage resistance in a marine cyanobacterium

Synechococcus is a significant primary producer in the oceans, coexisting with cyanophages which are important agents of mortality. Bacterial resistance against phage infection is a topic of significant interest, yet little is known for ecologically relevant systems. Here we use exogenous gene expression and gene disruption to investigate mechanisms underlying intracellular resistance of marine Synechococcus WH5701 to the Syn9 cyanophage. Despite possessing restriction-modification and Gabija defense systems, neither contributed to resistance. Instead, resistance was primarily driven by insufficient levels of LeuTAA tRNA, preventing translation of key phage genes in a passive, intracellular mode of resistance. Restoring cellular tRNA expression rendered the cyanobacterium sensitive to infection. We propose an evolutionary scenario whereby changes in cell codon usage, acquisition of tRNAs by the phage and loss of cell and phage tRNA expression resulted in an effective means of resistance, highlighting the dynamic interplay between bacteria and phages in shaping their co-evolutionary trajectories.

microbiology↗

bioRxiv2022

Siderophore production and utilization by microbes in the North Pacific Ocean

Siderophores are strong iron-binding molecules produced and utilized by microbes to acquire the limiting nutrient iron (Fe) from their surroundings. Despite their importance as a component of the iron-binding ligand pool in seawater, data on the distribution of siderophores and the microbes that use them are limited. Here we measured the concentrations and types of dissolved siderophores during two cruises in April 2016 and June 2017 that transited from the iron-replete, low-macronutrient North Pacific Subtropical Gyre (NPSG) through the North Pacific Transition Zone (NPTZ) to the iron-deplete, high-macronutrient North Pacific Subarctic Frontal Zone (SAFZ). Surface siderophore concentrations in 2017 were higher in the NPTZ (4.0 - 13.9 pM) than the SAFZ (1.2 - 5.1 pM), which may be partly attributed to stimulated siderophore production by environmental factors such as dust-derived iron concentrations (up to 0.51 nM). Multiple types of siderophores were identified on both cruises, including ferrioxamines, amphibactins and iron-free forms of photoreactive siderophores, which suggest active production and use of diverse siderophores across latitude and depth. Additionally, the widespread genetic potential for siderophore biosynthesis and uptake across latitude and the variability in the taxonomic composition of bacterial communities that transcribe putative ferrioxamine, amphibactin and salmochelin transporter genes at different latitudes suggest that particular microbes actively produce and use siderophores, altering siderophore distributions and the bioavailability of iron across the North Pacific.

ecology↗

bioRxiv2021

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↗

bioRxiv2018

Adaptation to sub-optimal hosts is a driver of viral diversification in the ocean

Marine cyanophages are viruses that infect oceanic cyanobacteria, thus affecting global ecological processes. Cyanophages of the Myoviridae family are of great interest since they include generalist viruses capable of infection of a wide range of hosts including those from different cyanobacterial genera. While the influence of phages on host evolution has been studied previously, it is not known how the infection of distinct hosts influences the evolution of cyanophage populations. In marine systems this question is of special interest as the abundance of different Synechococcus and Prochlorococcus hosts constantly changes, temporally and spatially. Here, using an experimental evolution approach, we investigated the adaptation of multiple cyanophage populations to three distinct cyanobacterial hosts. We show that when infecting an \"optimal\" host, whose infection is the most efficient, phage populations accumulated only a few mutations. However, when infecting \"sub-optimal\" hosts, different, largely host-specific sets of mutations, spread in the phage populations, leading to rapid diversification into distinct subpopulations. The mutations included insertions, deletions, SNPs and codon adaptations. Most of the mutations were found in genes encoding for proteins responsible for host recognition, attachment and infection, regardless of their evolutionary conservation. Based on our results, we propose a model demonstrating how shifts in bacterial abundance, which lead to infection of \"sub-optimal\" hosts, act as a driver for rapid diversification of phage populations.

evolutionary biology↗