Yoav Lehahn

Infection of phytoplankton by aerosolized marine viruses

Significance Marine viruses constitute a major ecological and evolutionary driving force in marine ecosystems and are responsible for cycling of major nutrients; however, their dispersal mechanisms remain underexplored. By using one of the most established host–pathogen planktonic model systems we provide strong evidence that specific viruses of marine coccolithophores can be transmitted and stay infective as marine aerosols. Being transported by the wind, phytoplankton viruses can be conveyed long distances and transmit the infection to remote locations to which coccolithophore blooms can be extended. We show that this effective transmission mechanism that has been studied in human, animal, and plant diseases could play an important role in host–virus dynamics during phytoplankton blooms in the ocean. 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.

Marine aerosol as a possible source for endotoxins in coastal areas

Marine aerosols, that are very common in the highly populated coastal cities and communities, may contain biological constituents. Some of this biological fraction of marine aerosols, such as cyanobacteria and plankton debris, may influence human health by inflammation and allergic reactions when inhaled. In this study we identify and compare sources for endotoxins sampled on filters in an on-shore and more-inland site. Filter analysis included endotoxin content, total bacteria, gram-negative bacteria and cyanobacteria genome concentrations as well as ion content in order to identify possible sources for the endotoxins. Satellite images of chlorophyll-a levels and back trajectory analysis were used to further study the cyanobacteria blooms in the sea, close to the trajectory of the sampled air. The highest endotoxin concentrations found in the shoreline site were during winter (3.23±0.17 EU/m(3)), together with the highest cyanobacteria genome (1065.5 genome/m(3)). The elevated endotoxin concentrations were significantly correlated with cyanobacterial levels scaled to the presence of marine aerosol (r=0.90), as well as to chlorophyll-a (r=0.96). Filters sampled further inland showed lower and non-significant correlation between endotoxin and cyanobacteria (r=0.70, P value=0.19), suggesting decrease in marine-originated endotoxin, with possible contributions from other sources of gram-negative non-cyanobacteria. We conclude that marine cyanobacteria may be a dominant contributor to elevated endotoxin levels in coastal areas.

Metagenomic analysis reveals unusually high incidence of proteorhodopsin genes in the ultraoligotrophic Eastern Mediterranean Sea

Sunlight can be directly harvested by photoheterotrophic bacteria to create a pH gradient across the membrane, which can then be utilized to produce ATP. Despite the potential importance of this trophic strategy, when and where such organisms are found in the seas and oceans is poorly described. Here, we describe the abundance and taxonomy of bacteria with different trophic strategies (heterotrophs, phototrophs and photoheterotrophs) in contrasting water masses of the ultra-oligotrophic eastern Mediterranean Sea. These water bodies, an anticyclonic eddy and a high-chlorophyll patch resulting from transport of nutrient-rich coastal waters into offshore oligotrophic waters, each supported different microbial populations in surface waters. Based on infrared microscopy and metagenomics, aerobic anoxygenic photoheterotrophic (AAP) bacteria represented up to 10.4% of the microbial community. In contrast, the proteorhodopsin (PR) gene was found in 78.6%-118.8% of the bacterial genome equivalents, the highest abundance reported to date. These results suggest that PR-mediated photoheterotrophy may be especially important in oligotrophic, potentially phosphate-limited conditions.

Coccolithovirus facilitation of carbon export in the North Atlantic

Marine phytoplankton account for approximately half of global primary productivity1, 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 carbon2, which can stimulate nutrient regeneration, primary production and upper ocean respiration2 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 ocean2. 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.Using a combination of remote-sensing technologies, lipidomics and gene-based biomarkers, the authors demonstrate a coupling between viral infection of an Emiliania huxleyi bloom and the export of organic and inorganic carbon from the photic zone.

Decoupling atmospheric and oceanic factors affecting aerosol loading over a cluster of mesoscale North Atlantic eddies

Using shipboard and satellite measurements we explore the environmental factors affecting the number concentration of aerosols with diameter 100 < D < 1000 nm over a cluster of three mesoscale (~10–100 km) eddies in the North Atlantic. Strongest sensitivity to environmental conditions was found in the 400 < D < 1000 nm size range. In this size range particle concentrations were closely linked to the surface wind speed, indicating in situ production of sea spray aerosols by wind-driven processes. Particle concentrations were also affected by mesoscale variability in oceanic conditions at the vicinity of an anticyclonic eddy. In addition, a distinct aerosol population possibly produced at a distance of ~1000–2000 km from the study area was identified. The results highlight the importance of oceanic and atmospheric mesoscale processes in determining the characteristics of aerosols over the marine environment.

Segmentation and Tracking of Marine Cellular Clouds observed by Geostationary Satellites

ABSTRACT Marine stratocumulus (MSC) are shallow marine boundary layer clouds that have a significant cooling contribution to the Earth’s radiative balance. The amplitude of this cooling effect strongly depends on the properties of closed and open cells comprising MSC cloud fields. Systematic study of the underlying processes associated with cloud cell properties requires accurate and reliable cell characterization. Here we propose a method for cell segmentation of MSC clouds as observed from geostationary satellite images. The method, which is based on watershed transformation, is found to be highly efficient in segmentation of both open and closed MSC scenes. Application of the suggested methodology over a Lagrangian framework that track the clouds as they are advected by the wind and comparison of the results between pairs of consecutive images indicate that the resulted segmentation is robust and consistent. The methodology developed in this work opens the way to systematic investigation of spatiotemporal changes in MSC cloud field properties, which will improve our understanding of MSC clouds and their role in regulating Earth’s radiative budget.

Expression profiling of host and virus during a coccolithophore bloom provides insights into the role of viral infection in promoting carbon export

The cosmopolitan coccolithophore Emiliania huxleyi is a unicellular eukaryotic alga that forms vast blooms in the oceans impacting large biogeochemical cycles. These blooms are often terminated due to infection by the large dsDNA virus, E. huxleyi virus (EhV). It was recently established that EhV-induced modulation of E. huxleyi metabolism is a key factor for optimal viral infection cycle. Despite the huge ecological importance of this host–virus interaction, the ability to assess its spatial and temporal dynamics and its possible impact on nutrient fluxes is limited by current approaches that focus on quantification of viral abundance and biodiversity. Here, we applied a host and virus gene expression analysis as a sensitive tool to quantify the dynamics of this interaction during a natural E. huxleyi bloom in the North Atlantic. We used viral gene expression profiling as an index for the level of active infection and showed that the latter correlated with water column depth. Intriguingly, this suggests a possible sinking mechanism for removing infected cells as aggregates from the E. huxleyi population in the surface layer into deeper waters. Viral infection was also highly correlated with induction of host metabolic genes involved in host life cycle, sphingolipid, and antioxidant metabolism, providing evidence for modulation of host metabolism under natural conditions. The ability to track and quantify defined phases of infection by monitoring co-expression of viral and host genes, coupled with advance omics approaches, will enable a deeper understanding of the impact that viruses have on the environment.

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.

A Satellite-Based Lagrangian View on Phytoplankton Dynamics

The well-lit upper layer of the open ocean is a dynamical environment that hosts approximately half of global primary production. In the remote parts of this environment, distant from the coast and from the seabed, there is no obvious spatially fixed reference frame for describing the dynamics of the microscopic drifting organisms responsible for this immense production of organic matter-the phytoplankton. Thus, a natural perspective for studying phytoplankton dynamics is to follow the trajectories of water parcels in which the organisms are embedded. With the advent of satellite oceanography, this Lagrangian perspective has provided valuable information on different aspects of phytoplankton dynamics, including bloom initiation and termination, spatial distribution patterns, biodiversity, export of carbon to the deep ocean, and, more recently, bottom-up mechanisms that affect the distribution and behavior of higher-trophic-level organisms. Upcoming submesoscale-resolving satellite observations and swarms of autonomous platforms open the way to the integration of vertical dynamics into the Lagrangian view of phytoplankton dynamics.