Geometric frustration in the myosin superlattice of vertebrate muscle

Millane, Rick P.; Wojtas, David H.; Hong Yoon, Chun; Blakeley, Nicholas D.; Bones, Philip J.; Goyal, Abhishek; Squire, John M.; Luther, Pradeep K.

doi:10.1098/rsif.2021.0585

Geometric frustration in the myosin superlattice of vertebrate muscle

Journal Article · Tue Dec 14 23:00:00 EST 2021 · Interface (Online)

DOI:https://doi.org/10.1098/rsif.2021.0585· OSTI ID:1865893

^[1]; Wojtas, David H. ^[1]; Hong Yoon, Chun ^[1]; Blakeley, Nicholas D. ^[1]; Bones, Philip J. ^[1]; Goyal, Abhishek ^[1]; Squire, John M. ^[2]; Luther, Pradeep K. ^[3]

Univ. of Canterbury, Christchurch (New Zealand)
Univ. of Bristol (United Kingdom)
Imperial College, London (United Kingdom)

Geometric frustration results from an incompatibility between minimum energy arrangements and the geometry of a system, and gives rise to interesting and novel phenomena. Here, we report geometric frustration in a native biological macromolecular system---vertebrate muscle. We analyse the disorder in the myosin filament rotations in the myofibrils of vertebrate striated (skeletal and cardiac) muscle, as seen in thin-section electron micrographs, and show that the distribution of rotations corresponds to an archetypical geometrically frustrated system---the triangular Ising antiferromagnet. Spatial correlations are evident out to at least six lattice spacings. The results demonstrate that geometric frustration can drive the development of structure in complex biological systems, and may have implications for the nature of the actin--myosin interactions involved in muscle contraction. Identification of the distribution of myosin filament rotations with an Ising model allows the extensive results on the latter to be applied to this system. It shows how local interactions (between adjacent myosin filaments) can determine long-range order and, conversely, how observations of long-range order (such as patterns seen in electron micrographs) can be used to estimate the energetics of these local interactions. Furthermore, since diffraction by a disordered system is a function of the second-order statistics, the derived correlations allow more accurate diffraction calculations, which can aid in interpretation of X-ray diffraction data from muscle specimens for structural analysis.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Univ. of Canterbury, Christchurch (New Zealand)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); New Zealand Marsden Fund; British Heart Foundation; European MYORES Network

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1865893

Alternate ID(s):: OSTI ID: 1882941

Journal Information:: Interface (Online), Journal Name: Interface (Online) Journal Issue: 185 Vol. 18; ISSN 1742-5662

Publisher:: The Royal SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Supplementary material; Filament rotations; Original micrograph files from Geometric frustration in the myosin superlattice of vertebrate muscle Millane, Rick P.; Wojtas, David H.; Hong Yoon, Chun https://doi.org/10.6084/m9.figshare.17104659 The current record is supplemented by this text	text	January 2021
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Geometric frustration in the myosin superlattice of vertebrate muscle

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