Feeding Mechanisms in Phagotrophic Nanoflagellates: Predation in the Low Reynolds Number World

Pelagic waters are nutritionally poor, with food distributed in heterogeneous patches that rapidly dissipate into the diluted environment. Yet, these temporary nutrient-rich regions become hotspots of life. A drop of seawater can contain around a million bacteria cells, which have rapid growth rates and are efficient consumers of dissolved organic matter. Surprisingly, bacterioplankton populations remain mostly constant. This is primarily due to the top-down pressure of small abundant predators known as phagotrophic nanoflagellates. These single-cell organisms (protists), equipped with one or more flagella and ranging from 2 – 20 μm in size, play a key role in the ‘microbial loop’, i.e. an alternative energy pathway to the classic marine trophic chain (phytoplankton – copepod – small fish). As the main consumers of bacteria and picophytoplankton, phagotrophic nanoflagellates are essential to the marine carbon cycles and global biogeochemical processes.

To survive, flagellates need to clear a million times their own volume of water per day. However, the microscale world is physically counterintuitive: water becomes viscous and particle-particle contacts are constrained. So how do flagellates thrive in ‘sticky’, nutrient-poor waters? They generate feeding currents by beating the flagellum to draw prey toward them for subsequent captures and ingestions. Phagotrophic nanoflagellates display a variety of flagellar arrangements and feeding behaviors. Moreover, they are functionally and phylogenetically diverse. Despite their ecological significance, their feeding processes remain largely unexplored.

This thesis aims to mechanistically understand the diversity of predation strategies in phagotrophic nanoflagellates. It comprises three collaborative papers, each addressing specific aspects. First, we investigate the feeding behaviors of four species of stramenopiles that generate flow with a hairy flagellum. Second, we describe the predation modes of ‘typical excavates’ that feed through a ventral groove associated with a vaned flagellum. Lastly, we report, for the first time, the activity of the ‘wave’ in the ventral groove of excavates and study their prey size range. Feeding behaviors were recorded through high-speed video microscopy, and theoretical models and computational fluid dynamic simulations were used to study the flow-generating forces of the beating flagellum. This thesis provides a mechanistic insight into the functional morphology and functional responses of two taxonomic groups and opens up new avenues for understanding the ecological significance of their feeding processes. By shedding light on these processes, we can gain a deeper understanding of the role of phagotrophic nanoflagellates in aquatic ecosystems.