Fluid dynamics, ecology, and evolution of marine flagellates: Motility, foraging mechanisms, and defense strategies

Plants, animals and fungi are often mentioned as examples of eukaryotes diversity. This is reasonable as we, humans, interacts with them in our everyday life. However, as a wise fox said once to a little prince, the essential is invisible to the eyes. These groups are surely diverse, but if we were only addressing diversity in this way, we would extremely underestimate the real diversity “hidden” in the eukaryote Tree of Life (eToL). Unicellular eukaryotes, also known as protists, represent the bulk of most major groups of eukaryotes, whereas multicellular lineages are confined to small corners of the eToL.

Many unicellular eukaryotes are equipped with motile appendages, called flagella, through which they perform all the activities needed for survival such as locomotion, fluid transport, and sensory functions. Many flagellates inhabit aquatic environments and play a key role in marine food webs. For a long time, only a few species of flagellates have been studied and used as model organisms, such as the sea urchin sperm cells and the green algae Chlamydomonas reinhardtii. This “black box” approach has limited the understanding of flagellates and their role in food webs, as it ignores the high morphological and behavioral diversity found among species belonging to different branches of the eToL. During evolution, flagellates have been exposed to diverse environments with diverse risks and opportunities, and individuals have responded to it developing countless survival strategies, which resulted in different morphologies, flagellar arrangements, beat patterns, resource acquisition modes, and defense mechanisms against predation. If we lack information about their morphological and functional diversity, we lack the core knowledge to understand the role of these species in marine ecosystems, as their success is dependent on the trade-offs associated to their traits.

The research conducted at the Centre for Ocean Life aims to create and implement novel trait-based approaches to life in the ocean, with the overarching goal of developing a fundamental understanding and predictive capability of marine ecosystems. My PhD project contributes to this goal by studying with a mechanistic approach different flagellates species that play an important role in marine food webs. My research focused on one of the major aspects of marine flagellates, i.e. their motility and the fluid dynamics around beating flagella. Their flagellar activity is fundamental to carrying out all their vital functions, i.e. swimming, foraging, and avoiding predation (stealth), and often plays conflicting roles in these functions. Therefore, to understand the success of flagellates in marine ecosystem we need to observe and quantitatively characterize the flow fields generated by their flagellar activity, so that we can quantify benefits and costs of having a certain flagellar arrangement or beat pattern.

This contribution was achieved with three sub-projects, which resulted in three collaborative papers. The first investigated the capability to escape predator-generated feeding current in three species belonging to the Haptophyta group, described the escape mechanism and quantified the triggering fluid signal. The second investigated the feeding strategy of five species of ‘typical excavates’ that feed through feeding current directed within a ventral groove, generated by a vaned flagellum. Both escaping and feeding behaviors were recorded through high-speed video microscopy, and theoretical models and Computational Fluid Dynamic (CFD) simulations were used to describe the fluid dynamics around the whole cell architecture and the resulting flow-field. Lastly, we showed how Digital Holographic Microscopy (DHM) systems can be implemented for 3-dimensional tracking of flagellar activity in protists, implementing a novel DHM-based method to the case of a complex study organism, the stramenopile Pseudobodo sp. This thesis thus provides insights into the functional traits, resulting behaviors and fluid dynamics of flagellates belonging to three different taxonomic groups of the eToL (Haptophyta, Excavata, and Stramenopila), by investigating and quantitatively characterizing their escape strategies, foraging mechanism, and 3-dimensional beat patterns, respectively.