Biology subjects

Sheyn, U.

Publications and source records attributed to Sheyn, U..

7 recordsLinked to original sources

bioRxiv2026

A chimeric infection program and epigenetic conflict underpin endogenous giant virus latency

Giant endogenous viral elements (GEVEs) are ubiquitous in eukaryotic genomes, but how the virus adapts to the host and is capable of reactivation despite host defense mechanisms remains unclear. Here we examined this process in the green alga Chlamydomonas reinhardtii and its latent giant virus, punuivirus, which is integrated into the host genome. We reveal a chimeric genomic architecture in which punuivirus latency genes are enriched in spliceosomal introns and 6-methyladenine marks, mirroring host transcriptional regulation, while virulence genes are predominantly controlled by a conserved viral promoter. Using single-cell RNA-seq, we show that nearly 70% of cells express viral transcripts, but only a small subpopulation commits to viral production, expressing virulence genes with host transcriptional shutoff. Moreover, we find that the intact punuivirus GEVE remains refractory to host 5-methylcytosine (5mC) silencing, whereas a naturally occurring deletion variant is associated with widespread 5mC accumulation across the GEVE and elsewhere in the host genome. The deleted region encodes a highly expressed ten-eleven translocation dioxygenase (TET), and epigenetic profiling of intact and deletion strains implicates this GEVE gene in removing 5mC marks, thereby maintaining the virus in a transcriptionally permissive latent state. Our study provides novel insights into the molecular underpinnings of host-virus co-existence in a giant virus-alga interaction.

microbiology↗

bioRxiv2024

Latent infection of an active giant endogenous virus in a unicellular green alga

Latency is a common strategy in a wide range of viral lineages, but its prevalence in giant viruses remains unknown. Here we describe the activity and viral production from a 617 kbp integrated giant viral element in the model green alga Chlamydomonas reinhardtii. We resolve the integrated viral region using long-read sequencing and show that viral particles are produced and released in otherwise healthy cultures. A diverse array of viral-encoded selfish genetic elements are expressed during GEVE reactivation and produce proteins that are packaged in virions. In addition, we show that field isolates of Chlamydomonas sp. harbor latent giant viruses related to the C. reinhardtii GEVE that exhibit similar infection dynamics, demonstrating that giant virus latency is prevalent in natural host communities. Our work reports the largest temperate virus documented to date and the first active GEVE identified in a unicellular eukaryote, substantially expanding the known limits of viral latency.

microbiology↗

bioRxiv2022

Daily turnover of active giant virus infection during algal blooms revealed by single-cell transcriptomics

Viruses are the most abundant biological entity in the ocean and play a significant role in shaping the marine ecosystem. The past two decades have revealed an outstanding diversity of giant viruses infecting protists across the tree of life and, in particular, algae that form massive blooms in the ocean. Virus-induced bloom demise significantly impacts marine ecology and biogeochemistry, as well as the associated microbial community. Nevertheless, little is known about the infection dynamics of these giant viruses in the natural environment and their role in regulating algal blooms. Here, we provide evidence for a daily life cycle of giant viral infection in algal blooms by processing the transcriptome of over 12,000 single algal cells during different phases of interaction with their giant viruses. We revealed that viral infection occurs already at the exponential phase of the bloom and that the timing of infection can determine the magnitude of the bloom but not the fraction of infected cells. We further revealed that the same proportion of infected cells are in the early phase of the viral replication program (13.5%) throughout several consecutive days of the bloom, suggesting that a daily turnover of infection is at play during the bloom and demise phases of the algal population. This may imply that a continuous source of virocell-associated metabolites diffuses throughout the bloom succession and could fuel the microbial food webs. Finally, we link single cell infection state to host physiology and show that infected cells remained calcified even in the late stage of infection, contradicting common observation of bulk population in which viral infection is directly linked with decalcification. Together, these results highlight the importance of studying host-virus dynamics in natural populations at a single-cell resolution, which can provide a fresh view of the dynamics and propagation of viral infection. This approach will enable quantification of the impact of marine viruses on microbial food webs.

microbiology↗

bioRxiv2021

Nitrogen fixation in mesoscale eddies of the North Pacific Subtropical Gyre: patterns and mechanisms

1.Mesoscale eddies have been shown to support elevated dinitrogen (N2) fixation rates (NFRs) and abundances of N2-fixing microorganisms (diazotrophs), but the mechanisms underlying these observations are not well understood. We explored relationships among NFRs and cyanobacterial diazotroph abundances in eddy pairs of opposite polarity sampled in the North Pacific Subtropical Gyre and compared our observations to seasonal trends from the Hawaii Ocean Time-series (HOT) program. Consistent with previous reports, we found that NFRs were anomalously high for this region (up to 3.7-fold above previous monthly HOT observations) in the centers of the sampled anticyclones, coinciding with elevated abundances of Crocosphaera in the summertime. We then coupled our field-based observations, together with transcriptomic analyses of nutrient stress marker genes and ecological models, to evaluate potential mechanisms controlling diazotroph abundance and activity at the mesoscale. Specifically, we evaluated the role of biological (via estimates of growth and grazing rates) and physical controls on populations of Crocosphaera, Trichodesmium, and diatom symbionts. Our results suggest that increased Crocosphaera abundances associated with summertime anticyclones resulted from the alleviation of phosphate limitation, allowing cells to grow at rates exceeding grazing losses. In contrast, distributions of larger, buoyant taxa (Trichodesmium and diatom symbionts) appeared less affected by eddy-driven biological controls. Instead, they appeared driven by physical dynamics along frontal boundaries that separate cyclonic and anticyclonic eddies. Together, the interplay of eddy-specific changes in bottom-up control, top-down control, and the physical accumulation of cells likely explains the elevated diazotroph abundances and NFRs associated with anticyclones and eddy fronts.

ecology↗

bioRxiv2020

Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise

Marine viruses are considered as major evolutionary and biogeochemical drivers of microbial life, through metabolic reprogramming of their host and cell lysis that modulates nutrient cycling1, primary production and carbon export in the oceans2. Despite the fact that viruses are the most abundant biological entities in the marine environment, we still lack mechanistic and quantitative approaches to assess their impact on the marine food webs. Here, we provide the first quantification of active viral infection, during bloom succession of the cosmopolitan coccolithophore Emiliania huxleyi, by subcellular visualization of both virus and host transcripts on a single cell resolution across thousands of cells. Using this novel method, that we coined Virocell-FISH, we revealed that distinct transcriptional states co-exist during the infection dynamics, and that viral infection reached only a quarter of the E. huxleyi population although the bloom demised in a synchronized manner. Through a detailed laboratory time-course infection of E. huxleyi by its lytic large virus EhV, we quantitatively show that metabolically active infected cells chronically release viral particles, and that viral-induced lysis is not systematically accompanied by virion increase, thus challenging major assumptions regarding the life cycle of giant lytic viruses. Using Virocell-FISH, we could further assess in a new resolution, the level of viral infection in cell aggregates, a key ecosystem process that can facilitate carbon export to the deep ocean3. We project that our approach can be applied to diverse marine microbial systems, opening a mechanistic dimension to the study of host-pathogen interactions in the ocean. One Sentence SummaryQuantifying active viral infection in algal blooms

microbiology↗

bioRxiv2019

Tracking infection dynamics at single-cell level reveals highly resolved expression programs of a large virus infecting algal blooms

Nucleocytoplasmic large DNA viruses have the largest genomes among all viruses and infect diverse eukaryotes across various ecosystems, but their expression regulation and infection strategies are not well understood. We profiled single-cell transcriptomes of the worldwide-distributed microalga Emiliania huxleyi and its specific coccolithovirus responsible for massive bloom demise. Heterogeneity in viral transcript levels detected among single cells was used to reconstruct the viral transcriptional trajectory and to map cells along a continuum of infection states. This enabled identification of novel viral genetic programs, which are composed of five kinetic classes with distinct promoter elements. The infection substantially changed the host transcriptome, causing rapid shutdown of protein-encoding nuclear transcripts at the onset of infection, while the plastid and mitochondrial transcriptomes persisted to mid- and late stages, respectively. Single-cell transcriptomics thereby opens the way for tracking host-pathogen infection dynamics at high resolution within microbial communities in the marine environment.

microbiology↗

bioRxiv2018

Bacterial virulence against an oceanic bloom-forming phytoplankter is mediated by algal DMSP

Emiliania huxleyi is a bloom forming microalga that impacts the global sulfur cycle by producing large amounts of dimethylsulfoniopropionate (DMSP) and its volatile metabolic product dimethyl sulfide (DMS). Top-down regulation of E. huxleyi blooms is attributed to viruses and grazers, however, the possible involvement of algicidal bacteria in bloom demise is still elusive. We isolated from a North Atlantic E. huxleyi bloom a Roseobacter strain, Sulfitobacter D7, which exhibited algicidal effects against E. huxleyi upon co-culturing. Both the alga and the bacterium were found to co-occur during a natural E. huxleyi bloom, therefore establishing this host-pathogen system as an attractive, ecologically relevant model for studying alga-bacterium interaction in the oceans. During interaction, Sulfitobacter D7 consumed and metabolized algal DMSP to produce high amounts of methanethiol, an alternative product of DMSP catabolism. We revealed a unique strain-specific response, in which E. huxleyi strains that exuded higher amounts of DMSP were more susceptible to Sulfitobacter D7 infection. Intriguingly, exogenous application of DMSP enhanced bacterial virulence and induced susceptibility in a resistant algal strain to the bacterial pathogen. This DMSP-dependent pathogenicity was highly specific as compared to supplementation of propionate and glycerol. We propose a novel function for DMSP, in addition to its central role in mutualistic interactions, as a mediator of bacterial virulence that may regulate E. huxleyi blooms.

microbiology↗