Biological Rotary Nanomotors

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Background

Everyone knows the utility of rotary systems for harnessing and converting energy. The energy of flowing water is captured on a small scale by waterwheels and on a large scale by turbines in hydroelectric dams. Wind energy is captured on a small scale by windmills and on a large scale by extensive wind farms. In 1973 Howard Berg shocked the scientific world by claiming that bacteria swim by rotating rigid helical filaments. Experiments soon proved him right. That breakthrough ushered in almost fifty years of subsequent research in which it has been found that rotating molecular motors are ubiquitous in living organisms. This issue presents a comprehensive picture of the state-of-the-art knowledge about biological rotary nanomotors.

Bacteria mastered the capture of the potential energy of ions flowing across the cell membrane to rotate motors that drive a number of different processes in the cell billions of years ago. First discovered was the propulsion of swimming bacteria. A decade later Paul Boyer suggested that the F0F1 ATP synthase (and ATPase) is a rotary device, and that was shown to be true. ATP synthesis in almost all organisms depends on an F0F1 ATP synthase, which was inherited from bacteria by archaea, mitochondria, and chloroplasts (with a more distant 'cousin' in A 0A 1 . Gliding bacteria also use rotary motors for propulsion, and rotary motors in the cell membrane drive the transport of large substrates across the outer membrane of gram-negative bacteria. The rotation of the helical filaments of the archaella is driven by ATP hydrolysis, not an ion motive force, but they still rotate and are associated with the cell membrane. All of these different systems will be discussed in this issue in reviews written by the researchers who made the discoveries.

The specific topics that will be discussed are as follows: bacterial flagella (Pushkar Lele, editor); archaella(Mike Manson, editor); bacterial gliding motors (Beiyan Nan, editor); the Tol and Ton outer membrane transport systems (Mike Manson, editor); the FoF1 ATPase (Tom Duncan, editor). Jun Liu will serve as the cryo-EM/structural expert responsible for reviewing all of the structural work in the topics just outlined. The reviews are not intended to be comprehensive discussions of the literature in the respective areas but rather be designed to make the reader familiar with the most recent advances and to present perspectives about how research on each topic is likely to unfold over the next several decades.

This issue is dedicated to two great scientists who have been an inspiration to me, and who fostered my career in academic research. The first is Howard Berg, who made rotation in the biological world respectable. Howard had the audacity and insight to publish, together with Robert Anderson, “Bacteria swim by rotating their flagellar filaments” in Nature in October 1973. Rotation at the nanoscale was welcomed into the biological world, and my decision of where to do my postdoctoral studies was made. Rotating flagella have been the focus of my research for 46 years since I joined the Berg lab in 1975. The second is the late Timothy Hall, who as Head of the Department of Biology at Texas A&M University hired me to begin my independent academic career in January 1987. I remained in that Department for 32 years until my retirement in January 2019. It is in Tim’s memory that the Texas A&M Department of Biology has offered to sponsor this issue of Frontiers in Microbiology devoted to the current state of knowledge about rotary biological nanomotors. - Professor Michael D Manson

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Keywords: ATP Synthase, bacteria, archaea, rotary motors, flagella, archaella, gliding motors, FoF1 ATPase, energy-coupled outer membrane transport

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