Trypanosoma, Paramecium and Tetrahymena: From genomics to flagellar and ciliary structures and cytoskeleton dynamics

Abstract

Cilia and flagella play an important role in motility, sensory perception, and the life cycles of eukaryotes, from protists to humans. However, much critical information concerning cilia structure and function remains elusive. The vast majority of ciliary and flagellar proteins analyzed so far are evolutionarily conserved and play a similar role in protozoa and vertebrates. This makes protozoa attractive biological models for studying cilia biology. Research conducted on ciliated or flagellated protists may improve our general understanding of cilia protein composition, of cilia beating, and can shed light on the molecular basis of the human disorders caused by motile cilia dysfunction. The Symposium “From genomics to flagellar and ciliary structures and cytoskeleton dynamics” at ECOP2019 in Rome presented the latest discoveries about cilia biogenesis and the molecular mechanisms of ciliary and flagellum motility based on studies in Paramecium, Tetrahymena, and Trypanosoma. Here, we review the most relevant aspects presented and discussed during the symposium and add our perspectives for future research.

Introduction

Cilia and flagella are external cell protrusions supported by an organized microtubular skeleton. These organelles play an important role in motility, sensory perception, and in the life cycles of eukaryotes, ranging from protists to humans. Over the last 15 years, driven by advances in imaging techniques and in genomic and proteomic technologies, cilia have been dissected at both the structural and functional level. This revealed that the lack of or mutation of some ciliary proteins cause ciliopathies – diseases triggered by cilia and flagella dysfunction (Heydeck et al., 2018, Wiegering et al., 2018). Despite the ubiquity and importance of these organelles, much critical information concerning cilia structure and function remains elusive. Importantly, the vast majority of ciliary proteins analyzed so far are evolutionarily conserved and play the same role in the motile cilia of protozoa and vertebrates, including human. This makes protozoa attractive biological models for studying cilia biology (Fig. 1).

Furthermore, many protists can be genetically manipulated enabling both protein sub-cellular localization and function to be defined (Dave et al., 2009, Gaertig et al., 2013, Oberholzer et al., 2009, Dean et al., 2015). Fig. 2 shows examples of protozoa genetically modified with genes fused to a fluorescent protein that allow the localization of the tagged proteins. Experiments conducted on ciliated or flagellated protists may thus not only improve our general understanding of cilia protein composition and the molecular mechanisms that regulate cilia beating, but can also shed light on the basis of human disorders caused by a dysfunction of motile cilia. Protists are also models for understanding cytoskeleton dynamics: the Hippo signaling pathway that controls the size of organs in all animals, has been demonstrated to control cell polarity in ciliates and to specify the relative dimension of the anterior and posterior daughter cells during division (Soares et al. 2019).

The speakers of the symposium “From genomics to flagellar and ciliary structures and cytoskeleton dynamics” at ECOP2019 in Rome presented their latest discoveries about the molecular mechanisms of ciliary and flagellum motility from their studies in Paramecium, Tetrahymena, and Trypanosoma, including molecules that are connected to human cilia-related disorders, among them infertility. Furthermore, the speakers presented data showing that the analyses of the molecular signals which regulate cell polarity in ciliates are a valuable complement to the research performed in human cells. Here, we briefly review the most relevant aspects presented and discussed during the symposium.