Marine phytoplankton account for approximately half of global primary productivity , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon , which can stimulate nutrient regeneration, primary production and upper ocean respiration via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid- and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

Selection of microorganisms in marine sediment is shaped by energy-yielding electron acceptors for respiration that are depleted in vertical succession. However, some taxa have been reported to reflect past depositional conditions suggesting they have experienced weak selection after burial. In sediments underlying the Arabian Sea oxygen minimum zone (OMZ), we performed the first metagenomic profiling of sedimentary DNA at centennial-scale resolution in the context of a multi-proxy paleoclimate reconstruction. While vertical distributions of sulfate reducing bacteria and methanogens indicate energy-based selection typical of anoxic marine sediments, 5–15% of taxa per sample exhibit depth-independent stratigraphies indicative of paleoenvironmental selection over relatively short geological timescales. Despite being vertically separated, indicator taxa deposited under OMZ conditions were more similar to one another than those deposited in bioturbated intervals under intervening higher oxygen. The genomic potential for denitrification also correlated with palaeo-OMZ proxies, independent of sediment depth and available nitrate and nitrite. However, metagenomes revealed mixed acid and Entner-Dourdoroff fermentation pathways encoded by many of the same denitrifier groups. Fermentation thus may explain the subsistence of these facultatively anaerobic microbes whose stratigraphy follows changing paleoceanographic conditions. At least for certain taxa, our analysis provides evidence of their paleoenvironmental selection over the last glacial-interglacial cycle.

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Subsurface microbial communities are generally thought to be structured through in situ environmental conditions such as the availability of electron acceptors and donors and porosity, but recent studies suggest that the vertical distribution of a subset of subseafloor microbial taxa, which were present at the time of deposition, were selected by the paleodepositional environment. However, additional highly resolved temporal records of subsurface microbiomes and paired paleoenvironmental reconstructions are needed to justify this claim. Here, we performed a highly resolved shotgun metagenomics survey to study the taxonomic and functional diversity of the subsurface microbiome in Holocene sediments underlying the permanently stratified and anoxic Black Sea. Obligate aerobic bacteria made the largest contribution to the observed shifts in microbial communities associated with known Holocene climate stages and transitions. This suggests that the aerobic fraction of the subseafloor microbiome was seeded from the water column and did not undergo post‐depositional selection. In contrast, obligate and facultative anaerobic bacteria showed the most significant response to the establishment of modern‐day environmental conditions 5.2 ka ago that led to a major shift in planktonic communities and in the type of sequestered organic matter available for microbial degradation. No significant shift in the subseafloor microbiome was observed as a result of environmental changes that occurred shortly after the marine reconnection, 9 ka ago. This supports the general view that the marine reconnection was a gradual process. We conclude that a high‐resolution analysis of downcore changes in the subseafloor microbiome can provide detailed insights into paleoenvironmental conditions and biogeochemical processes that occurred at the time of deposition.

Summary 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.