Biological nanomotors with a revolution, linear, or rotation motion mechanism

Peixuan Guo, Hiroyuki Noji, Christopher Yengo, Zhengyi Zhao, Ian Graingei

Research output: Contribution to journalReview article

17 Citations (Scopus)

Abstract

The ubiquitous biological nanomotors were classified into two categories in the past: linear and rotation motors. In 2013, a third type of biomotor, revolution without rotation (http://rnanano.osu.edu/movie.html), was discovered and found to be widespread among bacteria, eukaryotic viruses, and double-stranded DNA (dsDNA) bacteriophages. This review focuses on recent findings about various aspects of motors, including chirality, stoichiometry, channel size, entropy, conformational change, and energy usage rate, in a variety of well-studied motors, including FoF1 ATPase, helicases, viral ds DNA-packaging motors, bacterial chromosome translocases, myosin, kinesin, and dynein. In particular, dsDNA translocases are used to illustrate how these features relate to the motion mechanism and how nature elegantly evolved a revolution mechanism to avoid coiling and tangling during lengthy dsDNA genome transportation in cell division. Motor chirality and channel size are two factors that distinguish rotation motors from revolution motors. Rotation motors use right-handed channels to drive the right-handed dsDNA, similar to the way a nut drives the bolt with threads in same orientation; revolution motors use left-handed motor channels to revolve the right-handed dsDNA. Rotation motors use small channels (<2 nm in diameter) for the close contact of the channel wall with single-stranded DNA (ssDNA) or the 2-nm dsDNA bolt; revolution motors use larger channels (>3 nm) with room for the bolt to revolve. Binding and hydrolysis of ATP are linked to different conformational entropy changes in the motor that lead to altered affinity for the substrate and allow work to be done, for example, helicase unwinding of DNA or translocase directional movement of DNA.

Original languageEnglish (US)
Pages (from-to)161-186
Number of pages26
JournalMicrobiology and Molecular Biology Reviews
Volume80
Issue number1
DOIs
StatePublished - Mar 1 2016

Fingerprint

DNA
Entropy
Bacterial Chromosomes
Dyneins
Kinesin
Nuts
Product Packaging
Motion Pictures
Myosins
Cell Division
Bacteriophages
Adenosine Triphosphatases
Hydrolysis
Adenosine Triphosphate
Genome
Viruses
Bacteria

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Molecular Biology
  • Immunology and Microbiology(all)
  • Infectious Diseases

Cite this

Guo, Peixuan ; Noji, Hiroyuki ; Yengo, Christopher ; Zhao, Zhengyi ; Graingei, Ian. / Biological nanomotors with a revolution, linear, or rotation motion mechanism. In: Microbiology and Molecular Biology Reviews. 2016 ; Vol. 80, No. 1. pp. 161-186.
@article{b4cceb3e8b7542649dc7f137ef5dceff,
title = "Biological nanomotors with a revolution, linear, or rotation motion mechanism",
abstract = "The ubiquitous biological nanomotors were classified into two categories in the past: linear and rotation motors. In 2013, a third type of biomotor, revolution without rotation (http://rnanano.osu.edu/movie.html), was discovered and found to be widespread among bacteria, eukaryotic viruses, and double-stranded DNA (dsDNA) bacteriophages. This review focuses on recent findings about various aspects of motors, including chirality, stoichiometry, channel size, entropy, conformational change, and energy usage rate, in a variety of well-studied motors, including FoF1 ATPase, helicases, viral ds DNA-packaging motors, bacterial chromosome translocases, myosin, kinesin, and dynein. In particular, dsDNA translocases are used to illustrate how these features relate to the motion mechanism and how nature elegantly evolved a revolution mechanism to avoid coiling and tangling during lengthy dsDNA genome transportation in cell division. Motor chirality and channel size are two factors that distinguish rotation motors from revolution motors. Rotation motors use right-handed channels to drive the right-handed dsDNA, similar to the way a nut drives the bolt with threads in same orientation; revolution motors use left-handed motor channels to revolve the right-handed dsDNA. Rotation motors use small channels (<2 nm in diameter) for the close contact of the channel wall with single-stranded DNA (ssDNA) or the 2-nm dsDNA bolt; revolution motors use larger channels (>3 nm) with room for the bolt to revolve. Binding and hydrolysis of ATP are linked to different conformational entropy changes in the motor that lead to altered affinity for the substrate and allow work to be done, for example, helicase unwinding of DNA or translocase directional movement of DNA.",
author = "Peixuan Guo and Hiroyuki Noji and Christopher Yengo and Zhengyi Zhao and Ian Graingei",
year = "2016",
month = "3",
day = "1",
doi = "10.1128/MMBR.00056-15",
language = "English (US)",
volume = "80",
pages = "161--186",
journal = "Microbiology and Molecular Biology Reviews",
issn = "1092-2172",
publisher = "American Society for Microbiology",
number = "1",

}

Biological nanomotors with a revolution, linear, or rotation motion mechanism. / Guo, Peixuan; Noji, Hiroyuki; Yengo, Christopher; Zhao, Zhengyi; Graingei, Ian.

In: Microbiology and Molecular Biology Reviews, Vol. 80, No. 1, 01.03.2016, p. 161-186.

Research output: Contribution to journalReview article

TY - JOUR

T1 - Biological nanomotors with a revolution, linear, or rotation motion mechanism

AU - Guo, Peixuan

AU - Noji, Hiroyuki

AU - Yengo, Christopher

AU - Zhao, Zhengyi

AU - Graingei, Ian

PY - 2016/3/1

Y1 - 2016/3/1

N2 - The ubiquitous biological nanomotors were classified into two categories in the past: linear and rotation motors. In 2013, a third type of biomotor, revolution without rotation (http://rnanano.osu.edu/movie.html), was discovered and found to be widespread among bacteria, eukaryotic viruses, and double-stranded DNA (dsDNA) bacteriophages. This review focuses on recent findings about various aspects of motors, including chirality, stoichiometry, channel size, entropy, conformational change, and energy usage rate, in a variety of well-studied motors, including FoF1 ATPase, helicases, viral ds DNA-packaging motors, bacterial chromosome translocases, myosin, kinesin, and dynein. In particular, dsDNA translocases are used to illustrate how these features relate to the motion mechanism and how nature elegantly evolved a revolution mechanism to avoid coiling and tangling during lengthy dsDNA genome transportation in cell division. Motor chirality and channel size are two factors that distinguish rotation motors from revolution motors. Rotation motors use right-handed channels to drive the right-handed dsDNA, similar to the way a nut drives the bolt with threads in same orientation; revolution motors use left-handed motor channels to revolve the right-handed dsDNA. Rotation motors use small channels (<2 nm in diameter) for the close contact of the channel wall with single-stranded DNA (ssDNA) or the 2-nm dsDNA bolt; revolution motors use larger channels (>3 nm) with room for the bolt to revolve. Binding and hydrolysis of ATP are linked to different conformational entropy changes in the motor that lead to altered affinity for the substrate and allow work to be done, for example, helicase unwinding of DNA or translocase directional movement of DNA.

AB - The ubiquitous biological nanomotors were classified into two categories in the past: linear and rotation motors. In 2013, a third type of biomotor, revolution without rotation (http://rnanano.osu.edu/movie.html), was discovered and found to be widespread among bacteria, eukaryotic viruses, and double-stranded DNA (dsDNA) bacteriophages. This review focuses on recent findings about various aspects of motors, including chirality, stoichiometry, channel size, entropy, conformational change, and energy usage rate, in a variety of well-studied motors, including FoF1 ATPase, helicases, viral ds DNA-packaging motors, bacterial chromosome translocases, myosin, kinesin, and dynein. In particular, dsDNA translocases are used to illustrate how these features relate to the motion mechanism and how nature elegantly evolved a revolution mechanism to avoid coiling and tangling during lengthy dsDNA genome transportation in cell division. Motor chirality and channel size are two factors that distinguish rotation motors from revolution motors. Rotation motors use right-handed channels to drive the right-handed dsDNA, similar to the way a nut drives the bolt with threads in same orientation; revolution motors use left-handed motor channels to revolve the right-handed dsDNA. Rotation motors use small channels (<2 nm in diameter) for the close contact of the channel wall with single-stranded DNA (ssDNA) or the 2-nm dsDNA bolt; revolution motors use larger channels (>3 nm) with room for the bolt to revolve. Binding and hydrolysis of ATP are linked to different conformational entropy changes in the motor that lead to altered affinity for the substrate and allow work to be done, for example, helicase unwinding of DNA or translocase directional movement of DNA.

UR - http://www.scopus.com/inward/record.url?scp=84964068517&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84964068517&partnerID=8YFLogxK

U2 - 10.1128/MMBR.00056-15

DO - 10.1128/MMBR.00056-15

M3 - Review article

VL - 80

SP - 161

EP - 186

JO - Microbiology and Molecular Biology Reviews

JF - Microbiology and Molecular Biology Reviews

SN - 1092-2172

IS - 1

ER -