Abstract
Bacterial flagella are reversible rotary motors that rotate external filaments for bacterial propulsion. Some flagellar motors have diversified by recruiting additional components that influence torque and rotation, but little is known about the possible diversification and evolution of core motor components. The mechanistic core of flagella is the cytoplasmic C ring, which functions as a rotor, directional switch, and assembly platform for the flagellar type III secretion system (fT3SS) ATPase. The C ring is composed of a ring of FliG proteins and a helical ring of surface presentation of antigen (SPOA) domains from the switch proteins FliM and one of two usually mutually exclusive paralogs, FliN or FliY. We investigated the composition, architecture, and function of the C ring of Campylobacter jejuni, which encodes FliG, FliM, and both FliY and FliN by a variety of interrogative approaches. We discovered a diversified C. jejuni C ring containing FliG, FliM, and both FliY, which functions as a classical FliN-like protein for flagellar assembly, and FliN, which has neofunctionalized into a structural role. Specific protein interactions drive the formation of a more complex heterooligomeric C. jejuni C-ring structure. We discovered that this complex C ring has additional cellular functions in polarly localizing FlhG for numerical regulation of flagellar biogenesis and spatial regulation of division. Furthermore, mutation of the C. jejuni C ring revealed a T3SS that was less dependent on its ATPase complex for assembly than were other systems. Our results highlight considerable evolved flagellar diversity that impacts motor output, biogenesis, and cellular processes in different species.IMPORTANCE The conserved core of bacterial flagellar motors reflects a shared evolutionary history that preserves the mechanisms essential for flagellar assembly, rotation, and directional switching. In this work, we describe an expanded and diversified set of core components in the Campylobacter jejuni flagellar C ring, the mechanistic core of the motor. Our work provides insight into how usually conserved core components may have diversified by gene duplication, enabling a division of labor of the ancestral protein between the two new proteins, acquisition of new roles in flagellar assembly and motility, and expansion of the function of the flagellum beyond motility, including spatial regulation of cell division and numerical control of flagellar biogenesis in C. jejuni Our results highlight that relatively small changes, such as gene duplications, can have substantial ramifications on the cellular roles of a molecular machine.
Highlights
Bacterial flagella are reversible rotary motors that rotate external filaments for bacterial propulsion
Flagellar motors across bacterial species have conserved core structures composed of proteins with conserved functions, recent findings have shown that some mbio.asm.org motors have recruited extra proteins to form additional structures that adapt and enhance motor function [6,7,8, 10]
Operonic, genetic, and in situ structural analyses, we show that the C. jejuni C ring contains a paralogous duplication of an ancestral FliN-like protein to yield contemporary FliN and FliY, with FliY retaining a function more similar to that of FliN from the well-studied peritrichous E. coli and Salmonella sp. motors, and FliN diverging to a more supporting role in preserving C-ring structure for flagellar rotation
Summary
Bacterial flagella are reversible rotary motors that rotate external filaments for bacterial propulsion. Proton flux through a ring of stator complexes exerts torque upon a rotor [2,3,4]; torque is transmitted through a rigid periplasmic rod and flexible surface hook to an extracellular flagellar filament that coils as a helical propeller for propulsion [1] This rotor and a switch component that controls the direction of motor rotation together form a cytoplasmic ring, the C ring [5]. Structural studies suggest that homologous surface presentation of antigen (SPOA) domains in the C terminus of FliM and FliN form a continuous spiral through FliM-FliN3 protomers that compose the lower rim of the C ring [31, 40] This region of the C ring is an assembly platform for integration of an ATPase complex into the fT3SS. The presence of both FliY and FliN SPOA-containing proteins in Epsilonproteobacteria prompts questions regarding the function and location of these proteins, how have they diverged relative to an ancestral FliN-like protein, and what selective benefits drove retention of two FliN/FliY-like proteins
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