Heterogeneity in cilia patterning enables multiple flow functions within a single cell

Abstract

Free-living unicellular organisms known as ciliates rely on fluid flows to perform essential functions. These flows emerge from the coordinated activity of thousands of cilia organized into arrays with highly diverse architectures. Despite the importance of mesoscale cilia organization for flow generation, the relationship between the architecture of the ciliary array and the flow function it performs remains poorly understood. Here, we investigate how the ciliary array in the ciliate Paramecium tetraurelia enables this organism to feed and swim simultaneously. Using expansion microscopy and high-speed imaging, we measure ciliary organization and kinematics, from individual beat dynamics to collective metachronal wave patterns. We find that the cells surface is partitioned into arrays with distinct spatio-temporal patterns that perform specific functions. In addition to the oral apparatus, there are two structurally different domains: a densely ciliated high-frequency beating region located anterior to the oral apparatus and a second domain covering the remainder of the cells surface where cilia are more sparsely distributed and slower-beating. Selective removal of each region results in impaired feeding or swimming, demonstrating the functional specialization of each domain. Together, our findings show that a continuous cilia array can generate flows that perform different functions by locally encoding different ciliary architectures. More broadly, this work highlights spatio-temporal ciliary patterning as a key determinant of array function and provides insight into how organization of ciliary arrays governs swimming and transport in biological systems.