Disentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre.

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers in this environment function as the predominant top-down factor despite high standing viral particle densities. The model-data fits also reveal the ecological relevance of light-dependent viral traits and non-canonical factors to cellular loss. Finally, we leverage sensitivity analyses to demonstrate how variation in life history traits across distinct oceanic contexts, including variation in viral adsorption and grazer clearance rates, can transform the quantitative and even qualitative importance of top-down controls in shaping Prochlorococcus population dynamics.

Empirical relationship between nifH gene abundance and diazotroph cell concentration in the North Pacific Subtropical Gyre.

Cyanobacterial N2 -fixing microorganisms (diazotrophs) play a critical role in nitrogen and carbon cycling in the oceans; hence, accurate measurements of diazotroph abundance are imperative for understanding ocean biogeochemistry. Marine diazotroph abundances are often assessed using qPCR of the nifH gene, a sensitive, taxa-specific, and time/cost-efficient method. However, the validity of nifH abundance as a proxy for cell concentration has recently been questioned. Here, we compare nifH gene abundances to cell counts for four diazotroph taxa (Trichodesmium, Crocosphaera, Richelia, and Calothrix) on two cruises to the North Pacific Subtropical Gyre, one of the largest habitats for marine diazotrophs. nifH:cell relationships were strong and significant for Crocosphaera, Richelia, and Calothrix (nifH:cell 1.51-2.58; R2  = 0.89-0.96) but were not significant for Trichodesmium, despite previous studies reporting significant nifH:cell relationships for this organism. Limited available data suggest that empirical nifH:cell can vary among studies but that relationships are usually significantly linear and >1:1. Our study indicates that nifH gene abundance, while not a direct measure of cells, is a useful quantitative proxy for diazotroph abundance.

A system of coordinated autonomous robots for Lagrangian studies of microbes in the oceanic deep chlorophyll maximum.

The deep chlorophyll maximum (DCM) layer is an ecologically important feature of the open ocean. The DCM cannot be observed using aerial or satellite remote sensing; thus, in situ observations are essential. Further, understanding the responses of microbes to the environmental processes driving their metabolism and interactions requires observing in a reference frame that moves with a plankton population drifting in ocean currents, i.e., Lagrangian. Here, we report the development and application of a system of coordinated robots for studying planktonic biological communities drifting within the ocean. The presented Lagrangian system uses three coordinated autonomous robotic platforms. The focal platform consists of an autonomous underwater vehicle (AUV) fitted with a robotic water sampler. This platform localizes and drifts within a DCM community, periodically acquiring samples while continuously monitoring the local environment. The second platform is an AUV equipped with environmental sensing and acoustic tracking capabilities. This platform characterizes environmental conditions by tracking the focal platform and vertically profiling in its vicinity. The third platform is an autonomous surface vehicle equipped with satellite communications and subsea acoustic tracking capabilities. While also acoustically tracking the focal platform, this vehicle serves as a communication relay that connects the subsea robot to human operators, thereby providing situational awareness and enabling intervention if needed. Deployed in the North Pacific Ocean within the core of a cyclonic eddy, this coordinated system autonomously captured fundamental characteristics of the in situ DCM microbial community in a manner not possible previously.

Diel variability of bulk optical properties associated with the growth and division of small phytoplankton in the North Pacific Subtropical Gyre.

Cross-platform observing systems are requisite to capturing the temporal and spatial dynamics of particles in the ocean. We present simultaneous observations of bulk optical properties, including the particulate beam attenuation (cp) and backscattering (bbp) coefficients, and particle size distributions collected in the North Pacific Subtropical Gyre. Clear and coherent diel cycles are observed in all bulk and size-fractionated optical proxies for particle biomass. We show evidence linking diurnal increases in cp and bbp to daytime particle growth and division of cells, with particles <7µm driving the daily cycle of particle production and loss within the mixed layer. Flow cytometry data reveal the nitrogen-fixing cyanobacterium Crocosphaera (∼4-7µm) to be an important driver of cp at the time of sampling, whereas Prochlorococcus dynamics (∼0.5µm) were essential to reproducing temporal variability in bbp. This study is a step towards improved characterization of the particle size range represented by in situ bulk optical properties and a better understanding of the mechanisms that drive variability in particle production in the oligotrophic open ocean.

Kilauea lava fuels phytoplankton bloom in the North Pacific Ocean.

From June to August 2018, the eruption of Kilauea volcano on the island of Hawai'i injected millions of cubic meters of molten lava into the nutrient-poor waters of the North Pacific Subtropical Gyre. The lava-impacted seawater was characterized by high concentrations of metals and nutrients that stimulated phytoplankton growth, resulting in an extensive plume of chlorophyll a that was detectable by satellite. Chemical and molecular evidence revealed that this biological response hinged on unexpectedly high concentrations of nitrate, despite the negligible quantities of nitrogen in basaltic lava. We hypothesize that the high nitrate was caused by buoyant plumes of nutrient-rich deep waters created by the substantial input of lava into the ocean. This large-scale ocean fertilization was therefore a unique perturbation event that revealed how marine ecosystems respond to exogenous inputs of nutrients.

Evolution of the scattering properties of phytoplankton cells from flow cytometry measurements.

After the exponential growth phase, variability in the scattering efficiency of phytoplankton cells over their complete life cycle is not well characterised. Bulk measurements are impacted by senescent cells and detritrus. Thus the analysis of the evolution of the optical properties thanks to their morphological and/or intra-cellular variations remains poorly studied. Using the Cytosense flow cytometer (CytoBuoy b.v., NL), the temporal course of the forward and sideward efficiencies of two phytoplankton species (Thalassiosira pseudonana and Chlamydomonas concordia) were analyzed during a complete life-cycle. These two species differ considerably from a morphological point of view. Over the whole experiment, the forward and sideward efficiencies of Thalassiosira pseudonana were, on average, respectively 2.2 and 1.6 times higher than the efficiencies of Chlamydomonas concordia. Large intra-species variability of the efficiencies were observed over the life cycle of the considered species. It highlights the importance of considering the optical properties of phytoplankton cells as a function of the population growth stage of the considered species. Furthermore, flow cytometry measurements were combined with radiative transfer simulations and biogeochemical and optical measurements. Results showed that the real refractive index of the chloroplast is a key parameter driving the sideward signal and that a simplistic two-layered model (cytoplasm-chloroplast) seems particularly appropriate to represent the phytoplankton cells.

Consequence of a sudden wind event on the dynamics of a coastal phytoplankton community: an insight into specific population growth rates using a single cell high frequency approach.

Phytoplankton is a key component in marine ecosystems. It is responsible for most of the marine primary production, particularly in eutrophic lagoons, where it frequently blooms. Because they are very sensitive to their environment, the dynamics of these microbial communities has to be observed over different time scales, however, assessment of short term variability is often out of reach of traditional monitoring methods. To overcome these limitations, we set up a Cytosense automated flow cytometer (Cytobuoy b.v.), designed for high frequency monitoring of phytoplankton composition, abundance, cell size, and pigment content, in one of the largest Mediterranean lagoons, the Berre lagoon (South-Eastern France). During October 2011, it recorded the cell optical properties of 12 groups of pico-, nano-, and microphytoplankton. Daily variations in the cluster optical properties were consistent with individual changes observed using microscopic imaging, during the cell cycle. We therefore used an adaptation of the size-structured matrix population model, developed by Sosik et al. (2003) to process the single cell analysis of the clusters and estimate the division rates of 2 dinoflagellate populations before, during, and after a strong wind event. The increase in the estimated in situ daily cluster growth rates suggest that physiological changes in the cells can prevail over the response of abundance.

Seasonal distribution of ultraphytoplankton and heterotrophic prokaryotes in relation to abiotic variables on the north coast of Sfax after restoration.

The Taparura project was set up to restore the north Sfax coast (Tunisia) by shutting down the northern phosphate plant responsible for chronic pollution and uncontrolled phosphogypsum dumping. The restoration effect on coastal ultraphytoplankton (<10 µm) and heterotrophic prokaryotes was investigated using conventional flow cytometry over four successive seasons during 2009-2010. Cell concentrations were generally higher than values reported for the open sea, both in the western and eastern Mediterranean basins. One striking point was that chl a concentration on the north Sfax coast was unchanged after restoration but was still one order of magnitude higher than in the Gulf of Gabès. Restoration of pH, following the shutdown of the phosphate processing plants on the north coast, appeared to reach normal levels for seawater during the study, whereas seawater acidification persisted on the south coast where plants are still in operation. The largest ultraphytoplankton biomass was from an unknown cell group, whose identity and role needs to be established.