Discovery of a new motion mechanism of biomotors similar to the earth revolving around the sun without rotation

Abstract

Biomotors have been classified into linear and rotational motors. For 35 years, it has been popularly believed that viral dsDNA-packaging apparatuses are pentameric rotation motors. Recently, a third class of hexameric motor has been found in bacteriophage phi29 that utilizes a mechanism of revolution without rotation, friction, coiling, or torque. This review addresses how packaging motors control dsDNA one-way traffic; how four electropositive layers in the channel interact with the electronegative phosphate backbone to generate four steps in translocating one dsDNA helix; how motors resolve the mismatch between 10.5 bases and 12 connector subunits per cycle of revolution; and how ATP regulates sequential action of motor ATPase. Since motors with all number of subunits can utilize the revolution mechanism, this finding helps resolve puzzles and debates concerning the oligomeric nature of packaging motors in many phage systems. This revolution mechanism helps to solve the undesirable dsDNA supercoiling issue involved in rotation.

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

“…If this movement were correlated to ATP hydrolysis, it would provide a mechanism by which the protein could pump DNA. The translocation of dsDNA with 1.6 bp per subunit of FtsK (25,80) agrees well with the quantification for the phi29 DNA-packaging motor that each ATPase subunit uses one ATP to package 1.75 nucleotides (12,13,16,56,57) and for the bacteriophage T3 system with 1.8 bp per ATP (175). Based on these data, an inchworm mechanism has been proposed for FtsK (25,80), with ATPase subunits acting in a sequential manner.…”

“…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).…”

Finding of widespread viral and bacterial revolution dsDNA translocation motors distinct from rotation motors by channel chirality and size

“…Available evidences [58,60] lead to our hypothesis that FtsK and SpoIIIE motors also use a revolution mechanism to translocate dsDNA without rotation. Indeed, translocation of dsDNA by FtsK at a rate of 1.6-1.75 base per ATP [58,60] quantitatively agrees with the Phi29 DNA packaging motor in which each ATPase subunit uses one ATP to package 1.75 nucleotide [9,34,50,53,54]. Sequence studies of motor components of large eukaryotic dsDNA viruses, such as Acanthamoeba poylphaga mimivirus (APMV), and vaccinia viruses contain a dsDNA translocation motor that is similar to that of the FtsK-HerA superfamily [63,81,82], suggesting that these viruses also use the revolution mechanism for dsDNA packaging.…”

Single pore translocation of folded, double-stranded, and tetra-stranded DNA through channel of bacteriophage phi29 DNA packaging motor

“…Significant interactions are known to occur during the translocation process between the phosphate backbone of dsDNA and lysine residues of the connector channel [4,59]. Furthermore, the connector channel acts as a oneway valve with respect to dsDNA translocation [21].…”