Biology subjects

Schleyer, G.

Publications and source records attributed to Schleyer, G..

9 recordsLinked to original sources

bioRxiv2026

Viral infection and virophage co-infection induce distinct remodeling of host lipidome

Virophages are small double-stranded DNA viruses that co-infect eukaryotic cells along with giant viruses. They are widespread in aquatic ecosystems and can influence microbial population dynamics by acting as an adaptive antiviral defense system, limiting production of giant virus progeny. Giant viruses extensively reprogram host metabolism to support their replication, yet little is known about how this process is altered by virophages. Characterizing these alterations may reveal the metabolic mechanisms underlying virophage-mediated changes in infection outcomes. Here, we used one of the few established host-giant virus-virophage experimental systems, consisting of the marine heterotrophic flagellate Cafeteria burkhardae, its giant virus CroV, and the virophage mavirus, to investigate lipid remodeling during viral infection and virophage co-infection. We found that infection by the giant virus strongly induced triacylglycerols containing furan fatty acids (FuFAs), a class of potent antioxidants that may protect infected cells and newly formed virions from oxidative damage. These lipids were also detected in purified giant virus particles, linking their accumulation to virus production. Co-infection with the virophage reduced the FuFA response and was instead characterized by pronounced accumulation of the betaine lipid diacylglyceryltrimethylhomoserine (DGTS). Most of the induced DGTS species were also present in the giant virus particles, suggesting that their accumulation during co-infection may be associated with altered giant virus production and lipid utilization. Together, these findings show that virophage co-infection reshapes giant virus-induced remodeling of the host lipidome, revealing a potential metabolic basis for their effects on virus production and infection outcomes.

microbiology↗

bioRxiv2025

Synergy in viral-bacterial coinfection expedites algal bloom demise

Algal blooms are hotspots for diverse microbial interactions affecting bloom dynamics. Viral infections often regulate the demise of these blooms, recycling >25% of oceanic fixed carbon. Although these blooms collapse synchronously, only 10-30% of algal cells show active viral infection, suggesting additional mortality agents. Using microbial communities from natural coccolithophore blooms, we discovered that bacteria significantly enhanced virus-mediated algal mortality. We quantified this interaction using two novel metrics: the Synergy Index (SI) measuring viral-bacterial interaction strength, and the Benefit Index (BI) assessing changes in bacterial fitness. We identified Alteromonas bacteria as drivers of viral-bacterial coinfection with consistently high SI and BI. In natural communities, Alteromonas exhibited chemoattraction towards infected algal cells, leading to their enrichment in bloom demise particles. This viral-bacterial synergy represents a previously unrecognized mortality agent controlling bloom termination, modulating the balance between the carbon-recycling viral shunt and the carbon-exporting viral shuttle pathways, likely influencing global carbon cycling.

microbiology↗

bioRxiv2024

Mapping of the viral shunt across widespread coccolithophore blooms using metabolic biomarkers

The viral shunt is a fundamental ecosystem process which diverts the flux of organic carbon from grazers to heterotrophic microorganisms. Through the extracellular release of metabolites, lytic viral infections supply 2-10% of photosynthetically fixed carbon in the ocean for bacterial respiration. Despite its significance for the carbon cycle, we lack tools to detect the viral shunt in the natural environment and assess its ecological impact. Here, we study the use of exometabolites as biomarkers for the viral shunt by applying molecular, metabolomics, and oceanographic tools in blooms of the cosmopolitan microalga Gephyrocapsa huxleyi across the Atlantic Ocean, spanning four biogeochemical provinces between Iceland and Patagonia. We mapped the distinct metabolic footprint of its viral infections using exo- and endometabolomics approaches and detected nineteen organohalogen metabolites across the blooms, showing their global formation. Time-resolved comparison of particulate and dissolved metabolite pools during an induced mesocosm bloom indicated virocells - actively infected host cells - as the source of the halogenated metabolites. Three trichloro-iodo metabolites were present during demise of all virus-infected blooms, highlighting them as suitable metabolic biomarkers. The environmental stability of these halometabolites in the DOM pool over a few days can recapitulate viral infections at earlier stages of phytoplankton bloom succession.

ecology↗

bioRxiv2023

Cell-to-cell heterogeneity drives host-virus coexistence in a bloom-forming alga

Algal blooms drive global biogeochemical cycles of key nutrients in the oceans and serve as hotspots for biological interactions. The massive spring blooms of the cosmopolitan coccolithophore Emiliania huxleyi (E. huxleyi) are often infected by the lytic Emiliania huxleyi specific virus (EhV) which is a major mortality agent triggering bloom demise. Nonetheless, the multi-annual "boom and bust" pattern of E. huxleyi suggests that mechanisms of coexistence are essential for these host-virus dynamics. To investigate host-virus coexistence, we developed a new model system from an E. huxleyi culture which recovered from viral infection. The recovered population coexists with the virus, as host cells continue to grow in parallel to viral production. By applying a single-molecule fluorescence in situ hybridization (smFISH) approach to quantify the fraction of infected cells and assessing infection-specific lipid biomarkers, we identified a small subpopulation (5-7% of cells) that was infected and produced new virions, whereas the majority of the host population could resist infection. To further assess population heterogeneity, we generated monoclonal strain collections using single-cell sorting and subsequently phenotyped their susceptibility to EhV infection. This unraveled a substantial cell-to-cell heterogeneity across a continuum of susceptibility to resistance, suggesting that infection outcomes may vary depending on the individual cell. These results add a new dimension to our understanding of the complexity of host-virus interactions that are commonly assessed in bulk and described by binary definitions of resistance or susceptibility. We propose that phenotypic heterogeneity drives E. huxleyi-EhV coexistence and may potentially provide the coexisting strain an ecological advantage by killing competing susceptible strains.

microbiology↗

bioRxiv2022

Novel lipid biomarkers for algal resistance to viral infection in the ocean

Marine viruses play a key role in regulating phytoplankton populations, greatly affecting the biogeochemical cycling of major nutrients in the ocean. Resistance to viral infection has been reported for various phytoplankton species under laboratory conditions. Nevertheless, the occurrence of resistant cells in natural populations is underexplored due to the lack of sensitive tools to detect these rare phenotypes. Consequently, our current understanding of the ecological importance of resistance and its underlying mechanisms is limited. Here, we sought to discover lipid biomarkers for the resistance of the bloom-forming alga Emiliania huxleyi to its specific virus, E. huxleyi virus (EhV). We identified novel glycosphingolipids (GSLs) that characterize resistant E. huxleyi strains by applying an untargeted lipidomics approach. Further, we detected these lipid biomarkers in E. huxleyi isolates that were recently collected from E. huxleyi blooms and used them to detect resistant cells in the demise phase of an open ocean E. huxleyi bloom. Lastly, we show that the GSL composition of E. huxleyi cultures that recover following infection and gain resistance to the virus resembles that of resistant strains. These findings highlight the metabolic plasticity and co-evolution of the GSL biosynthetic pathway and underscore its central part in this host-virus arms race.

microbiology↗

bioRxiv2021

Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during algal blooms

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global nutrient cycling. When blooms collapse, organic carbon is transferred to higher trophic levels, microbial respiration or sinking in proportions that depend on the dominant mortality agent. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains an open question. Here, we characterized the consequences of viral infection on the microbiome composition and biogeochemical landscape of marine ecosystems by conducting a large-scale mesocosm experiment. Moniroting of seven induced coccolithophore blooms, which showed different degrees of viral infection, revealed that only high levels of viral infection caused significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, viral infection favored the growth of eukaryotic heterotrophs (thraustochytrids) over bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection can increase per-cell rates of extracellular carbon release by 2-4.5 fold. This happened via production of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms.

microbiology↗

bioRxiv2021

The ecological significance of extracellular vesicles in modulating host-virus interactions during algal blooms

Extracellular vesicles are produced by organisms from all kingdoms and serve a myriad of functions, many of which involve cell-cell signaling, especially during stress conditions and host-pathogen interactions. In the marine environment, communication between microorganisms can shape trophic level interactions and population succession, yet we know very little about the involvement of vesicles in these processes. In a previous study, we showed that vesicles produced during viral infection by the ecologically important model alga Emiliania huxleyi, could act as a pro-viral signal, by expediting infection and enhancing the half-life of the virus in the extracellular milieu. Here, we expand our laboratory findings and show the effect of vesicles on natural populations of E. huxleyi in a mesocosm setting. We profile the small-RNA (sRNA) cargo of vesicles that were produced by E. huxleyi during bloom succession, and show that vesicles applied to natural assemblages expedite viral infection and prolong the half-life of this major mortality agent of E. huxleyi. We subsequently reveal that exposure of the natural assemblage to E. huxleyi-derived vesicles modulates not only host-virus dynamics, but also other components of the microbial food webs, thus emphasizing the importance of extracellular vesicles to microbial interactions in the marine environment.

microbiology↗

bioRxiv2020

Viral infection of algal blooms leaves a halogenated footprint on the dissolved organic matter in the ocean

Algal blooms are important hotspots of primary production in the ocean, forming the basis of the marine food web and fueling the pool of dissolved organic matter (DOM)1, which is the largest global inventory of reduced carbon and a market place for metabolic exchange in the ocean2. Marine viruses are key players in controlling algal bloom demise and act as major biogeochemical drivers of nutrient cycling and metabolic fluxes by shunting algal biomass from higher trophic levels to the DOM pool, a process termed the viral shunt3,4. Nevertheless, the metabolic composition of virus-induced DOM (vDOM) in the marine environment is unknown. To decode the metabolic footprint of the viral shunt, we induced a bloom of the ecologically important alga Emiliania huxleyi in the natural environment, and followed its succession using an untargeted exometabolomics approach. Here we show that algal bloom succession induces extensive and dynamic changes in the exometabolic landscape, especially during bloom demise. By correlating to a specific viral gene marker, we discovered a set of novel chlorine-iodine-containing metabolites that were induced by viral infection and copiously released during bloom demise. We further detected several of these chloro-iodo metabolites in virus-infected open ocean blooms of E. huxleyi, supporting their use as sensitive biomarkers for virus-induced demise in the natural environment. Therefore, we propose halogenation to be a hallmark of the E. huxleyi vDOM, providing insights into the profound metabolic consequences of viral infection for the marine DOM pool.

microbiology↗

bioRxiv2018

\"In plaque-mass spectrometry imaging\" reveals a major metabolic shift towards odd-chain fatty acid lipids induced by host-virus interactions

Tapping into the metabolic cross-talk between a host and its virus can reveal unique strategies employed during infection. Viral infection is a dynamic process that generates an evolving metabolic landscape. Gaining a continuous view into the infection process is highly challenging and is limited by current metabolomics approaches, which typically measure the average of the entire population at various stages of infection. Here, we took a novel approach to study the metabolic basis of host-virus interactions between the bloom-forming alga Emiliania huxleyi and its specific virus. We combined a classical method in virology, plaque assay, with advanced mass spectrometry imaging (MSI), an approach we termed in plaque-MSI. Taking advantage of the spatial characteristics of the plaque, we mapped the metabolic landscape induced during infection in a high spatiotemporal resolution, unfolding the infection process in a continuous manner. Further unsupervised spatially-aware clustering, combined with known lipid biomarkers, revealed a systematic metabolic shift towards lipids containing the odd-chain fatty acid pentadecanoic acid (C15:0) induced during infection. Applying in plaque-MSI might pave the way for the discovery of novel bioactive compounds that mediate the chemical arms race of host-virus interactions in diverse model systems.

microbiology↗