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Actomyosin rings are specializations of the nonmuscle actomyosin cytoskeleton that drive cell shape changes during division, wound healing, and other events. Contractile rings throughout phylogeny and in a range of cellular contexts are built from conserved components, including nonmuscle myosin II, actin filaments, and cross-linking proteins. To explore whether diverse actomyosin rings generate contractile force and close via a common mechanism, we studied three instances of ring closure within the continuous cytoplasm of the Caenorhabditis elegans syncytial oogenic germline: mitotic cytokinesis of germline stem cells, apoptosis of meiotic compartments, and cellularization of oocytes. The three ring types exhibited distinct closure kinetics and component protein abundance dynamics. We formulated a physical model to relate measured closure speed and molecular composition dynamics to ring active stress and viscosity. We conclude that these ring intrinsic factors vary among the ring types. Our model suggests that motor and nonmotor cross-linkers’ abundance and distribution along filaments are important to recapitulate observed closure dynamics. Thus, our findings suggest that across ring closure contexts, fundamental contractile mechanics are conserved, and the magnitude of contractile force is tuned via regulation of ring component abundance and distribution. These results motivate testable hypotheses about cytoskeletal regulation, architecture, and remodeling. 

Summary The non-muscle actomyosin cytoskeleton generates contractile force through the dynamic rearrangement of its constituent parts. Actomyosin rings are a specialization of the non-muscle actomyosin cytoskeleton that drive cell shape changes during division, wound healing, and other events. Contractile rings throughout phylogeny and in a range of cellular contexts are built from conserved components including non-muscle myosin II (NMMII), actin filaments (F-actin), and crosslinking proteins. However, it is unknown whether diverse actomyosin rings close via a single unifying mechanism. To explore how contractile forces are generated by actomyosin rings, we studied three instances of ring closure within the common cytoplasm of theC. elegansoogenic germline: mitotic cytokinesis of germline stem cells (GSCs), apoptosis of meiotic compartments, and cellularization of oocytes. We found that each ring type closed with unique kinetics, protein density and abundance dynamics. These measurements suggested that the mechanism of contractile force generation varied across the subcellular contexts. Next, we formulated a physical model that related the forces generated by filament-filament interactions to the material properties of these rings that dictate the kinetics of their closure. Using this framework, we related the density of conserved cytoskeletal proteins anillin and NMMII to the kinematics of ring closure. We fitted model rings to in situ measurements to estimate parameters that are currently experimentally inaccessible, such as the asymmetric distribution of protein along the length of F-actin, which occurs naturally due to differences in the dimensions of the crosslinker and NMMII filaments. Our work predicted that the role of NMMII varies across these ring types, due in part to its distribution along F-actin and motoring. Our model also predicted that the degree of contractility and the impact of ring material properties on contractility differs among ring types.