Geologic controls on phytoplankton elemental composition.

Planktonic organic matter forms the base of the marine food web, and its nutrient content (C:N:Porg) governs material and energy fluxes in the ocean. Over Earth history, C:N:Porg had a crucial role in marine metazoan evolution and global biogeochemical dynamics, but the geologic history of C:N:Porg is unknown, and it is often regarded constant at the "Redfield" ratio of ∼106:16:1. We calculated C:N:Porg through Phanerozoic time by including nutrient- and temperature-dependent C:N:Porg parameterizations in a model of the long-timescale biogeochemical cycles. We infer a decrease from high Paleozoic C:Porg and N:Porg to present-day ratios, which stems from a decrease in the global average temperature and an increase in seawater phosphate availability. These changes in the phytoplankton's growth environment were driven by various Phanerozoic events: specifically, the middle to late Paleozoic expansion of land plants and the Triassic breakup of the supercontinent Pangaea, which increased continental weatherability and the fluxes of weathering-derived phosphate to the oceans. The resulting increase in the nutrient content of planktonic organic matter likely impacted the evolution of marine fauna and global biogeochemistry.

Geologic controls on phytoplankton elemental composition.

Planktonic organic matter forms the base of the marine food web, and its nutrient content (C:N:Porg) governs material and energy fluxes in the ocean. Over Earth history, C:N:Porg had a crucial role in marine metazoan evolution and global biogeochemical dynamics, but the geologic history of C:N:Porg is unknown, and it is often regarded constant at the "Redfield" ratio of ∼106:16:1. We calculated C:N:Porg through Phanerozoic time by including nutrient- and temperature-dependent C:N:Porg parameterizations in a model of the long-timescale biogeochemical cycles. We infer a decrease from high Paleozoic C:Porg and N:Porg to present-day ratios, which stems from a decrease in the global average temperature and an increase in seawater phosphate availability. These changes in the phytoplankton's growth environment were driven by various Phanerozoic events: specifically, the middle to late Paleozoic expansion of land plants and the Triassic breakup of the supercontinent Pangaea, which increased continental weatherability and the fluxes of weathering-derived phosphate to the oceans. The resulting increase in the nutrient content of planktonic organic matter likely impacted the evolution of marine fauna and global biogeochemistry.

Nutrient ratios in marine particulate organic matter are predicted by the population structure of well-adapted phytoplankton.

A common assumption of a constant nitrogen-to-phosphorus ratio (N:P) of 16:1 in marine particulate organic matter (POM) appears to be invalidated by observations of major spatial variations in N:P. Two main explanations have been proposed. The first attributes the N:P variability to changes in the community composition of well-adapted phytoplankton. The second proposes that variability arises from physiological acclimation involving intracellular adjustments of nutrient allocation under nutrient deficiency. Using a model of phytoplankton physiology, observational datasets, and a review of laboratory culture results, we assess the mechanistic basis of N:P variability. We find that the taxonomic composition of well-adapted phytoplankton best explains observed variations in POM N:P. Furthermore, we show that acclimation to nutrient deficiency may be safely neglected when considering the effects of ecology on POM N:P. These findings provide insight into the controls on global variability in POM composition and average phytoplankton physiological performance in the oceans.

Infection Dynamics of a Bloom-Forming Alga and Its Virus Determine Airborne Coccolith Emission from Seawater.

Sea spray aerosols (SSA), have a profound effect on the climate; however, the contribution of oceanic microbial activity to SSA is not fully established. We assessed aerosolization of the calcite units (coccoliths) that compose the exoskeleton of the cosmopolitan bloom-forming coccolithophore, Emiliania huxleyi. Airborne coccolith emission occurs in steady-state conditions and increases by an order of magnitude during E. huxleyi infection by E. huxleyi virus (EhV). Airborne to seawater coccolith ratio is 1:108, providing estimation of airborne concentrations from seawater concentrations. The coccoliths' unique aerodynamic structure yields a characteristic settling velocity of ∼0.01 cm s-1, ∼25 times slower than average sea salt particles, resulting in coccolith fraction enrichment in the air. The calculated enrichment was established experimentally, indicating that coccoliths may be key contributors to coarse mode SSA surface area, comparable with sea salt aerosols. This study suggests a coupling between key oceanic microbial interactions and fundamental atmospheric processes like SSA formation.

Dispersion/dilution enhances phytoplankton blooms in low-nutrient waters.

Spatial characteristics of phytoplankton blooms often reflect the horizontal transport properties of the oceanic turbulent flow in which they are embedded. Classically, bloom response to horizontal stirring is regarded in terms of generation of patchiness following large-scale bloom initiation. Here, using satellite observations from the North Pacific Subtropical Gyre and a simple ecosystem model, we show that the opposite scenario of turbulence dispersing and diluting fine-scale (∼1-100 km) nutrient-enriched water patches has the critical effect of regulating the dynamics of nutrients-phytoplankton-zooplankton ecosystems and enhancing accumulation of photosynthetic biomass in low-nutrient oceanic environments. A key factor in determining ecological and biogeochemical consequences of turbulent stirring is the horizontal dilution rate, which depends on the effective eddy diffusivity and surface area of the enriched patches. Implementation of the notion of horizontal dilution rate explains quantitatively plankton response to turbulence and improves our ability to represent ecological and biogeochemical processes in oligotrophic oceans.

Infection of phytoplankton by aerosolized marine viruses.

Marine viruses constitute a major ecological and evolutionary driving force in the marine ecosystems. However, their dispersal mechanisms remain underexplored. Here we follow the dynamics of Emiliania huxleyi viruses (EhV) that infect the ubiquitous, bloom-forming phytoplankton E. huxleyi and show that EhV are emitted to the atmosphere as primary marine aerosols. Using a laboratory-based setup, we showed that the dynamic of EhV aerial emission is strongly coupled to the host-virus dynamic in the culture media. In addition, we recovered EhV DNA from atmospheric samples collected over an E. huxleyi bloom in the North Atlantic, providing evidence for aerosolization of marine viruses in their natural environment. Decay rate analysis in the laboratory revealed that aerosolized viruses can remain infective under meteorological conditions prevailing during E. huxleyi blooms in the ocean, allowing potential dispersal and infectivity over hundreds of kilometers. Based on the combined laboratory and in situ findings, we propose that atmospheric transport of EhV is an effective transmission mechanism for spreading viral infection over large areas in the ocean. This transmission mechanism may also have an important ecological impact on the large-scale host-virus "arms race" during bloom succession and consequently the turnover of carbon in the ocean.

Decoupling physical from biological processes to assess the impact of viruses on a mesoscale algal bloom.

Phytoplankton blooms are ephemeral events of exceptionally high primary productivity that regulate the flux of carbon across marine food webs [1-3]. Quantification of bloom turnover [4] is limited by a fundamental difficulty to decouple between physical and biological processes as observed by ocean color satellite data. This limitation hinders the quantification of bloom demise and its regulation by biological processes [5, 6], which has important consequences on the efficiency of the biological pump of carbon to the deep ocean [7-9]. Here, we address this challenge and quantify algal blooms' turnover using a combination of satellite and in situ data, which allows identification of a relatively stable oceanic patch that is subject to little mixing with its surroundings. Using a newly developed multisatellite Lagrangian diagnostic, we decouple the contributions of physical and biological processes, allowing quantification of a complete life cycle of a mesoscale (∼10-100 km) bloom of coccolithophores in the North Atlantic, from exponential growth to its rapid demise. We estimate the amount of organic carbon produced during the bloom to be in the order of 24,000 tons, of which two-thirds were turned over within 1 week. Complimentary in situ measurements of the same patch area revealed high levels of specific viruses infecting coccolithophore cells, therefore pointing at the importance of viral infection as a possible mortality agent. Application of the newly developed satellite-based approaches opens the way for large-scale quantification of the impact of diverse environmental stresses on the fate of phytoplankton blooms and derived carbon in the ocean.