Membrane-embedded molecular motors to propel microorganisms

Motor proteins are molecular machines that convert chemical energy into mechanical work.

Abstract

Motor proteins are molecular machines that convert chemical energy into mechanical work. In addition to existing studies performed on the linear motors found in eukaryotic cells, researchers in biophysics have also focused on rotary motors such as bacterial flagellar motor (BFM) and ATP synthase, both of which localize at cell membranes. The research group including Nishizaka contributed to correlate all chemical states to specific mechanical events in motors by visualizing single chemical reactions under the advanced optical microscope [1-3]. From the structural point of view, conformational changes of  catalytic subunit in the soluble subcomplex of ATP synthase, F1-ATPase, was directly visualized at the single molecular level [4,5]. Additionally, behaviors of the shaft were also addressed through a series of microscopy techniques [6,7]. Recent studies showed that there exists another ATP-driven protein motor in life: the rotary machinery that rotates archaeal flagella (archaella). None of the archaellar motility structure is homologous to any BMF proteins. Rotation speed, stepwise movement, and variable directionality of the motor of Halobacterium salinarum were described in previous studies [8]. We further presented recent experimental work discerning the molecular mechanism underlying how the archaellar motor protein FlaI drives rotation by generation of motor torque [9,10]. In combination, those studies found that rotation slows as the viscous drag of markers increases, but torque remains constant at 160 pN·nm independent of rotation speed. Unexpectedly, the estimated work done in a single rotation is twice the expected energy that would come from hydrolysis of six ATP molecules in the FlaI hexamer. To reconcile the apparent contradiction, a new and general model for the mechanism of ATP-driven rotary motors will be discussed.

References

  1. Nishizaka, T., K. Oiwa, H. Noji, S. Kimura, E. Muneyuki, M. Yoshida, and K. Kinosita, Jr.  Nature Struct. Mol. Biol. 11, 142-8 (2004)
  2. Adachi, K., K. Oiwa, T. Nishizaka, S. Furuike, H. Noji, H. Itoh, M. Yoshida, and K. Kinosita, Jr.  Cell 130, 309-21 (2007)
  3. Adachi, K., K. Oiwa, M. Yoshida, T. Nishizaka, and K. Kinosita, Jr.  Nature Commun. 3, 1022 (2012)
  4. Masaike, T., F. Koyama-Horibe, K. Oiwa, M. Yoshida, and T. Nishizaka.  Nature Struct. Mol. Biol. 15, 1326-33 (2008)
  5. Sugawa, M., K. Okazaki, M. Kobayashi, T. Matsui, G. Hummer, T. Masaike, and T. Nishizaka.  Proc. Natl. Acad. Sci. USA 113, E2916-24 (2016)
  6. Sugawa, M., K. A. Okada, T. Masaike, and T. Nishizaka.  Biophys. J. 101, 2201-6 (2011)
  7. Naito, T. M., T. Masaike, D. Nakane, M. Sugawa, K. A. Okada, and T. Nishizaka.  Sci. Rep. 9, 7451 (2019)
  8. Kinosita, Y., N. Uchida, D. Nakane, and T. Nishizaka.  Nature Microbiol. 1, 16148 (2016)
  9. Iwata, S., Y. Kinosita, N. Uchida, D. Nakane, and T. Nishizaka.  Commun. Biol. 2, 199 (2019)
  10.  Nishizaka, T., T. Masaike, and D. Nakane.  Biophys. Rev. 11, 653-57 (2019)

Biographical Sketch

Dr. Takayuki Nishizaka is a professor in the Physics Department of the historically celebrated Gakushuin University, the oldest private university in Japan, located in Tokyo. Gakushuin ranks first among all Japanese universities in quality of research in the natural sciences, and Prof. Nishizaka’s research in biophysics contributed to the high score (Nature 555, S73 (2018)).

Prof. Nishizaka received his PhD in physics from Waseda University in 1996. His research interests include molecular motors, cell motility and the development of advanced optical microscopes to study single protein molecules. His recent research topics include applications of microscope techniques to study the motility of various microorganisms. He contributed to the visualization of the mechanics and chemical reactions of single protein molecules in their native state, immobilized on glass. For this achievement, he was awarded the JSPS Prize in 2008, the most prestigious award in Japan for young researchers in the humanities, social sciences and natural sciences. He has published papers in top journals as the first author or corresponding author, including eight papers in  Nature and the Nature family journals, and four in PNAS. He also works as Administration Officer in Biophysical Society of Japan, and Executive Committee in Asian Biophysics Association.