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

Vincent, Flora; Gralka, Matti; Schleyer, Guy; Schatz, Daniella; Cabrera-Brufau, Miguel; Kuhlisch, Constanze; Sichert, Andreas; Vidal‐Melgosa, Silvia; Mayers, Kyle; Barak-Gavish, Noa; Flores, Juana M.; Masdeu-Navarro, Marta; Egge, Jorun K.; Larsen, Aud; Heheman, Jan-Hendrick; Marrasé, Cèlia; Simó, Rafel; Cordero, Otto X.; Vardi, Assaf

doi:10.21203/rs.3.rs-1045578/v1

Cited by 5 publications

(1 citation statement)

References 62 publications

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“…Phycoerythrin was detected by FL3 (ex: 488 nm and em: 570 to 620 nm). Raw.fcs files were extracted and analyzed in R using "flowCore" and "ggcyto" packages, and all data are available on Dryad (57).…”

Section: Flow Cytometry Measurementsmentioning

confidence: 99%

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

Hevroni,

Vincent,

et al. 2023

Sci. Adv.

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Giant viruses infect many unicellular eukaryotes, including algae that form massive oceanic blooms. Despite the major impact of viruses on the marine ecosystem, the ability to quantify and assess active viral infection in nature remains a major challenge. We applied single-cell RNA sequencing, to profile virus and host transcriptomes of 12,000 single algal cells from a coccolithophore bloom. Viral infection was detected already at early exponential bloom phase, negatively correlating with the bloom intensity. A consistent percent of infected coccolithophores displayed the early phase of viral replication for several consecutive days, indicating a daily turnover and continuous virocell-associated metabolite production, potentially affecting the surrounding microbiome. Linking single-cell infection state to host physiology revealed that infected cells remained calcified even in the late infection stage. These findings stress the importance of studying host-virus dynamics in natural populations, at single-cell resolution, to better understand virus life cycle and its impact on microbial food webs.

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Section: Flow Cytometry Measurementsmentioning

confidence: 99%

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

Hevroni,

Vincent,

et al. 2023

Sci. Adv.

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Bacterial lifestyle switch in response to algal metabolites

Barak-Gavish

Dassa

Kuhlisch

et al. 2022

Preprint

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Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly recognized that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during its interaction with Emiliania huxleyi, a cosmopolitan bloom-forming phytoplankter. To unravel the bacterial lifestyle switch, we profiled bacterial transcriptomes in response to infochemicals derived from algae in exponential and stationary growth, which induced the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. We found that algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. In the pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and many transport systems, presumably to maximize assimilation of E. huxleyi-derived metabolites released by algal cells upon cell death. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7, and negated the DMSP-inducing lifestyle switch to pathogenicity, demonstrating that benzoate is important for maintaining the coexistence of algae and bacteria. We propose that bacteria can sense the physiological status of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during the interactions.

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

Schleyer

Kuhlisch

Ziv

et al. 2022

Preprint

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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.

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

Cited by 5 publications

References 62 publications

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

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

Bacterial lifestyle switch in response to algal metabolites

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

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