Plastic cell morphology changes during dispersal

Abstract

Summary Dispersal is the movement of organisms from one habitat to another that potentially results in gene flow. It is often plastic, allowing organisms to adjust dispersal movements depending on environmental conditions. A fundamental aim in ecology is to understand the determinants underlying dispersal and its plasticity. We utilized 22 strains of the ciliate Tetrahymena thermophila to determine if different phenotypic dispersal strategies co-exist within a species and which mechanisms underlie this variability. We quantified the cell morphologies impacting cell motility and dispersal. Distinct differences in innate cellular morphology and dispersal rates were detected, but no universally utilized combinations of morphological parameters correlate with dispersal. Rather, multiple distinct and plastic morphological changes impact cilia-dependent motility during dispersal, especially in proficient dispersing strains facing challenging environmental conditions. Combining ecology and cell biology experiments, we show that dispersal can be promoted through plastic motility-associated changes to cell morphology and motile cilia.

Ciliate cortical organization and dynamics for cell motility: Comparing ciliates and vertebrates

“…Consistent with this, low nutrient conditions induce Tetrahymena cells to enter a dispersal state whereby they remodel their cell cortex (Nelsen, 1978;Nelsen & Debault, 1978). Dispersing Tetrahymena cells, known as dispersers, undergo morphological changes that include shorter cell length and more closely positioned cilia within ciliary rows (Figure 6; Junker et al, 2021;Nelsen, 1978). Reduced cilia spacing is typically associated with faster fluid flow (Elgeti & Gompper, 2013;Gu et al, 2020;Osterman & Vilfan, 2011).…”

“…Reduced cilia spacing is typically associated with faster fluid flow (Elgeti & Gompper, 2013;Gu et al, 2020;Osterman & Vilfan, 2011). Consistent with this, dispersers swim at faster rates than resident Tetrahymena cells (Junker et al, 2021). Thus, the Tetrahymena cell cortex reorganizes its BBs and cilia under nutrient poor conditions to promote dispersal (Junker et al, 2021;Nelsen, 1978).…”

“…In nutrient poor conditions, dispersing Tetrahymena cells increase their number of cilia by promoting ciliogenesis at unciliated BBs (Nelsen, 1978). The increase in cilia number facilitates faster cell motility, which is one of the characteristics of dispersing Tetrahymena cells (Junker et al, 2021;Omori et al, 2020). In addition, a subpopulation of dispersers generates an additional extended cilium, referred to as the caudal cilium, which is positioned on the posterior cell pole (Figure 6A; Nelsen, 1978).…”

“…In addition, a subpopulation of dispersers generates an additional extended cilium, referred to as the caudal cilium, which is positioned on the posterior cell pole (Figure 6A; Nelsen, 1978). The caudal cilium is variable in length, and it is approximately 1.2-to 2.3-fold longer than the average motile cilium that is positioned at the medial region of the cell (Junker et al, 2021). Although its role is unclear, the caudal cilium is speculated to function as a rudder for steering function (Nelsen, 1978).…”

“…Harsh environments like poor nutrient conditions often drive organisms, including Tetrahymena, to enter a state of dispersal whereby they migrate, colonize new and favorable habitats, and promote gene flow (Figure 6A; Jacob et al, 2017;Van Dyck & Baguette, 2005). Ecology studies revealed that a dispersing individual possesses unique morphological traits that distinguish it from a non-dispersing, or resident, individual (Clobert et al, 2009;Jacob et al, 2019;Junker et al, 2021;Stevens et al, 2013). Consistent with this, low nutrient conditions induce Tetrahymena cells to enter a dispersal state whereby they remodel their cell cortex (Nelsen, 1978;Nelsen & Debault, 1978).…”