Coccolithophores fix organic carbon and produce calcite plates (coccoliths) that ballast organic matter and facilitate carbon export. Photosynthesis consumes carbon dioxide, while calcification produces it, raising questions about whether coccolithophores are a net sink or source of carbon. We characterized the physiology of calcified and noncalcified ("naked") phenotypes of Emiliania huxleyi (CCMP374) and investigated the relationship between calcification and photosynthesis across a gradient of light (25-2000 mu mol photons m(-2) s(-1)) spanning the euphotic zone. Growth and photophysiological parameters increased with light until reaching a mid-light (150 mu mol photons m(-2) s(-1)) maximum for both phenotypes. Calcified cells were characterized by enhanced photophysiology and less photoinhibition. Further, enhanced bicarbonate transport in calcified cells led to higher rates of particulate organic carbon fixation and growth compared to naked cells at mid-light to high light (150-2000 mu mol photons m(-2) s(-1)). Coccolith production was similarly high at mid and high light, but the rate of coccolith shedding was >3-fold lower at high-light (1.2 vs. 0.35 coccoliths cell(-1) h(-1)). The cellular mechanims(s) of this differential shedding remain unknown and underly light-related controls on coccosphere maintenance. Our data suggest coccoliths shade cells at high light and that enhanced bicarbonate transport associated with calcification increases internal carbon supplies available for organic carbon fixation.

Marine coccolithophores are globally distributed, unicellular phytoplankton that produce nanopatterned, calcite biominerals (coccoliths). These biominerals are synthesized internally, deposited into an extracellular coccosphere, and routinely released into the external medium, where they profoundly affect the global carbon cycle. The cellular costs and benefits of calcification remain unresolved. Here, we show observational and experimental evidence, supported by biophysical modeling, that free coccoliths are highly adsorptive biominerals that readily interact with cells to form chimeric coccospheres and with viruses to form “viroliths,” which facilitate infection. Adsorption to cells is mediated by organic matter associated with the coccolith base plate and varies with biomineral morphology. Biomineral hitchhiking increases host-virus encounters by nearly an order of magnitude and can be the dominant mode of infection under stormy conditions, fundamentally altering how we view biomineral-cell-virus interactions in the environment.

Interactions between marine viruses and microbes are a critical part of the oceanic carbon cycle. The impacts of virus-host interactions range from short-term disruptions in the mobility of microbial biomass carbon to higher trophic levels through cell lysis (i.e., the viral shunt) to long-term reallocation of microbial biomass carbon to the deep sea through accelerating the biological pump (i.e., the viral shuttle). The biogeochemical backdrop of the ocean-the physical, chemical, and biological landscape-influences the likelihood of both virus-host interactions and particle formation, and the fate and flow of carbon. As climate change reshapes the oceanic landscape through large-scale shifts in temperature, circulation, stratification, and acidification, virus-mediated carbon flux is likely to shift in response. Dynamics in the directionality and magnitude of changes in how, where, and when viruses mediate the recycling or storage of microbial biomass carbon is largely unknown. Integrating viral infection dynamics data obtained from experimental models and field systems, with particle motion microphysics and global observations of oceanic biogeochemistry, into improved ecosystem models will enable viral oceanographers to better predict the role of viruses in marine carbon cycling in the future ocean.

Raw data for "Seasonal mixed layer depth shapes phytoplankton physiology, viral production, and accumulation in the North Atlantic".

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus-host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host-virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host-virus densities.

Coccolithoviruses (EhVs) are large, double-stranded DNA-containing viruses that infect the single-celled, marine coccolithophore Emiliania huxleyi. Given the cosmopolitan nature and global importance of E. huxleyi as a bloom-forming, calcifying, photoautotroph, E. huxleyi-EhV interactions play a key role in oceanic carbon biogeochemistry. Virally-encoded glycosphingolipids (vGSLs) are virulence factors that are produced by the activity of virus-encoded serine palmitoyltransferase (SPT). Here, we characterize the dynamics, diversity and catalytic production of vGSLs in an array of EhV strains in relation to their SPT sequence composition and explore the hypothesis that they are a determinant of infectivity and host demise. vGSL production and diversity was positively correlated with increased virulence, virus replication rate and lytic infection dynamics in laboratory experiments, but they do not explain the success of less-virulent EhVs in natural EhV communities. The majority of EhV-derived SPT amplicon sequences associated with infected cells in the North Atlantic derived from slower infecting, less virulent EhVs. Our lab-, field- and mathematical model-based data and simulations support ecological scenarios whereby slow-infecting, less-virulent EhVs successfully compete in North Atlantic populations of E. huxleyi, through either the preferential removal of fast-infecting, virulent EhVs during active infection or by having access to a broader host range.

Two prominent characteristics of marine coccolithophores are their secretion of coccoliths and their susceptibility to infection by coccolithoviruses (EhVs), both of which display variation among cells in culture and in natural populations. We examined the impact of calcification on infection by challenging a variety of Emiliania huxleyi strains at different calcification states with EhVs of different virulence. Reduced cellular calcification was associated with increased infection and EhV production, even though calcified cells and associated coccoliths had significantly higher adsorption coefficients than non-calcified (naked) cells. Sialic acid glycosphingolipids, molecules thought to mediate EhV infection, were generally more abundant in calcified cells and enriched in purified, sorted coccoliths, suggesting a biochemical link between calcification and adsorption rates. In turn, viable EhVs impacted cellular calcification absent of lysis by inducing dramatic shifts in optical side scatter signals and a massive release of detached coccoliths in a subpopulation of cells, which could be triggered by resuspension of healthy, calcified host cells in an EhV-free, 'induced media'. Our findings show that calcification is a key component of the E. huxleyi-EhV arms race and an aspect that is critical both to the modelling of these host-virus interactions in the ocean and interpreting their impact on the global carbon cycle.

Emiliania huxleyi produces calcium carbonate (CaCO3 ) coccoliths and transparent exopolymer particles (TEP), sticky, acidic carbohydrates that facilitate aggregation. E. huxleyi's extensive oceanic blooms are often terminated by coccolithoviruses (EhVs) with the transport of cellular debris and associated particulate organic carbon (POC) to depth being facilitated by TEP-bound 'marine snow' aggregates. The dynamics of TEP production and particle aggregation in response to EhV infection are poorly understood. Using flow cytometry, spectrophotometry and FlowCam visualization of alcian blue (AB)-stained aggregates, we assessed TEP production and the size spectrum of aggregates for E. huxleyi possessing different degrees of calcification and cellular CaCO3 :POC mass ratios, when challenged with two EhVs (EhV207 and EhV99B1). FlowCam imaging also qualitatively assessed the relative amount of AB-stainable TEP (i.e., blue:red ratio of each particle). We show significant increases in TEP during early phase EhV207-infection (∼ 24 h) of calcifying strains and a shift towards large aggregates following EhV99B1-infection. We also observed the formation of large aggregates with low blue:red ratios, suggesting that other exopolymer substances contribute towards aggregation. Our findings show the potential for virus infection and the associated response of their hosts to impact carbon flux dynamics and provide incentive to explore these dynamics in natural populations.