The efficiency of the ocean’s biological carbon pump is mediated by fast-sinking particles that quickly settle out of the euphotic zone. These particles are conventionally associated with micro- (> 20 µm) sized diatoms and coccolithophorids, thought to efficiently transport carbon to depth owing to their dense mineral structures, while pico- (< 2 µm) and nanophytoplankton (2-20 µm) are considered to contribute negligibly due to their small size and low sinking speed. Despite burgeoning evidence of their export, the mechanisms behind it remain poorly understood. The objective of this dissertation is to acquire a mechanistic understanding of the contribution of pico- and nanophytoplankton to particle fluxes. I tested the hypotheses that pico- and nanophytoplankton may be exported via the following pathways: 1) physical aggregation due to the production of sticky Transparent Exopolymeric Particles (TEP), mediated by interactions with heterotrophic bacteria, 2) attachment to lithogenic minerals, and 3) repackaging by zooplankton. I found that despite the traditional view of being too small to sink, pico- and nanophytoplankton form aggregates rich in TEP, allowing cells to scavenge lithogenic minerals and thus increase their effective size and density. I discovered that interactions with heterotrophic bacteria were significant in mediating the process of aggregation by influencing the production and/or the composition of the phytoplankton-derived TEP. Bacteria differentially influenced aggregation and TEP production; some species enhanced aggregation without affecting TEP production, and vice-versa. Finally, by determining the microbial composition of sinking particles in an open-ocean site, I found pico- and nanophytoplankton significantly associated with particles sourced from crustaceous zooplankton, suggesting that their export is largely mediated by mesozooplankton. Overall, I show that the hypothesized mechanisms of pico- and nanophytoplankton export are not mutually exclusive, but instead occur subsequently. Given the right conditions for their aggregation in the natural environment, such as interactions with aggregation-enhancing heterotrophic bacteria and/or the presence of lithogenic minerals, their cells and aggregates can escape remineralization within the euphotic zone, and thus be susceptible to grazing by mesozooplankton export within fecal pellets. The results of this dissertation provide a mechanistic framework for the contribution of pico- and nanophytoplankton to ocean particle fluxes.

Marine pico-cyanobacteria of the genera Synechococcus and Prochlorococcus carry out nearly two thirds of the primary production in oligotrophic oceans. These cyanobacteria are also considered an important constituent of the biological carbon pump, the photosynthetic fixation of CO2 to dissolved and particulate organic carbon and subsequent export to the ocean’s interior. But single cells of these cyanobacteria are too small to sink, so their carbon export has to be mediated by aggregate formation and/or consumption by zooplankton that produce sinking fecal pellets. In this dissertation, I investigated for the first time the aggregation of these cyanobacteria by studying the marine Synechococcus sp. strain WH8102 as a model organism. I first found in culture experiments that Synechococcus cells aggregated and that such aggregation of cells was related to the production of transparent exopolymeric particles (TEP), known to provide the main matrix of aggregates of eukaryotic phytoplankton. I also found that despite the lowered growth rates, cells in the nitrogen or phosphorus limited cultures had a higher cell-normalized TEP production and formed a greater total volume of aggregates with higher settling velocities compared to cells in the nutrient replete cultures. I further studied the Synechococcus aggregation in roller tanks that allow the simulation of aggregates settling in the water column, and investigated the effects of the clays kaolinite and bentonite that are commonly found in the ocean. In the roller tanks, Synechococcus cells formed aggregates with diameters of up to 1.4 mm and sinking velocities of up to 440 m/d, comparable to those of larger eukaryotic phytoplankton such as diatoms. In addition, the clay minerals increased the number but reduced the size of aggregates, and their ballasting effects increased the sinking velocity and the carbon export potential of the aggregates. Lastly, I investigated the effects of heterotrophic bacteria on the Synechococcus aggregation, and found that heterotrophic bacteria generally resulted in the formation of fewer, but larger and faster sinking aggregates, and eventually led to an enhanced aggregation of cells and particles. My study contributes to the understanding of the role of marine pico-cyanobacteria in the ecology and biogeochemistry of oligotrophic oceans.