Common mechanisms of DNA translocation motors in bacteria and viruses using one-way revolution mechanism without rotation

Abstract

Biomotors were once classified into two categories: linear motor and rotation motor. For decades, the viral DNA-packaging motor has been popularly believed to be a five-fold rotation motor. Recently, a third type of biomotor with revolution mechanism without rotation has been discovered. By analogy, rotation resembles the Earth rotating on its axis in a complete cycle every 24 hours, while revolution resembles the Earth revolving around the Sun one circle per 365 days (see animations http://nanobio.uky.edu/movie.html). The action of revolution that enables a motor free of coiling and torque has solved many puzzles and debates that have occurred throughout the history of viral DNA packaging motor studies. It also settles the discrepancies concerning the structure, stoichiometry, and functioning of DNA translocation motors. This review uses bacteriophages Phi29, HK97, SPP1, P22, T4, T7 as well as bacterial DNA translocase FtsK and SpoIIIE as examples to elucidate the puzzles. These motors use a ATPase, some of which have been confirmed to be a hexamer, to revolve around the dsDNA sequentially. ATP binding induces conformational change and possibly an entropy alteration in ATPase to a high affinity toward dsDNA; but ATP hydrolysis triggers another entropic and conformational change in ATPase to a low affinity for DNA, by which dsDNA is pushed toward an adjacent ATPase subunit. The rotation and revolution mechanisms can be distinguished by the size of channel: the channels of rotation motors are equal to or smaller than 2 nm, whereas channels of revolution motors are larger than 3 nm. Rotation motors use parallel threads to operate with a right-handed channel, while revolution motors use a left-handed channel to drive the right-handed DNA in an anti-parallel arrangement. Coordination of several vector factors in the same direction makes viral DNA-packaging motors unusually powerful and effective. Revolution mechanism avoids DNA coiling in translocating the lengthy genomic dsDNA helix could be advantage for cell replication such as bacterial binary fission and cell mitosis without the need for topoisomerase or helicase to consume additional energy.

Non-monotonous polymer translocation time across corrugated channels: Comparison between Fick-Jacobs approximation and numerical simulations

“…Many biological processes such as viral injection of DNA into host cells [1,2], DNA transport through membrane or organelles [3] and gene transferring between bacteria [4,5] involve the translocation of bio-polymer through nano-channels and nano-pores. Moreover, due to technological applications such as polymer separation, DNA sequencing and protein sensing, polymer translocation phenomena has been largely investigated in recent years [6][7][8][9][10][11][12][13][14][15][16][17][18][19][20].…”

Biological Nanomotors with a Revolution, Linear, or Rotation Motion Mechanism

“…Based on their motion mechanisms, the biomotors are categorized into three classes: linear, rotary, and revolutional ( Fig. 1) (8)(9)(10)(11)(12)(13)(14)(15)(16). Rotation is the circular movement of an object around its own axis, resembling the Earth rotating on its axis in a complete cycle every 24 h. Revolution is the turning of an object around a second object, resembling the action of the Earth revolving around the sun one circle per year (Fig.…”

“…DNA was found to twist by as little as 1.5 degrees per base pair translocated, confirming a nonrotation mechanism (6), since 1.5°/bp ϫ 10.5 bp/helical turn ϭ 15.7°is far below the 360°per complete helical turn. This puzzle of "rotation motors that do not rotate" was not solved until the breakthrough of the discovery of revolution motion in 2013 by Guo's group (12)(13)(14)(15)(16) (Fig. 5).…”

“…(Adapted from reference 50 and adapted from reference 15 with permission from Elsevier.) tive subunit of the phage phi29 DNA-packaging motor completely blocks the function of the ATPase ring (12,13,15,56).…”

Development of Potent Antiviral Drugs Inspired by Viral Hexameric DNA-Packaging Motors with Revolving Mechanism

“…Viral DNA packaging motors can generally be divided into two closely related categories (19): (i) terminase and portal channel-mediated DNA translocation, as in herpesviruses (20), adenoviruses (8), and many bacteriophages, including phi29 (21), T4 (22), T3 (23), T5 (24), T7 (25), (26), SPP1 (27), and HK97 (16,28), and (ii) HerA/FtsK-type translocase, as in poxvirus and other nucleocytoplasmic large DNA viruses (NCLDV) (29,30). Both categories use very similar revolving mechanisms (13,15,21,28).…”