Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component

Novelty in biology can arise from opportunistic repurposing of nascent characteristics of existing features. Understanding how this process happens at the molecular scale, however, suffers from a lack of case studies. The evolutionary emergence of rotary motors is a particularly clear example of evo...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Trishant R. Umrekar, Yvonne B. Winterborn, Shamphavi Sivabalasarma, Julian Brantl, Sonja-Verena Albers, Morgan Beeby
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	archaellar motor stator complex single particle analysis molecular evolution exaptation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a5938ca9cac74d69a5b262583537543f
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:a5938ca9cac74d69a5b262583537543f
record_format	dspace
spelling	oai:doaj.org-article:a5938ca9cac74d69a5b262583537543f2021-12-01T13:50:09ZEvolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component1664-302X10.3389/fmicb.2021.773386https://doaj.org/article/a5938ca9cac74d69a5b262583537543f2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.773386/fullhttps://doaj.org/toc/1664-302XNovelty in biology can arise from opportunistic repurposing of nascent characteristics of existing features. Understanding how this process happens at the molecular scale, however, suffers from a lack of case studies. The evolutionary emergence of rotary motors is a particularly clear example of evolution of a new function. The simplest of rotary motors is the archaellum, a molecular motor that spins a helical propeller for archaeal motility analogous to the bacterial flagellum. Curiously, emergence of archaellar rotation may have pivoted on the simple duplication and repurposing of a pre-existing component to produce a stator complex that anchors to the cell superstructure to enable productive rotation of the rotor component. This putative stator complex is composed of ArlF and ArlG, gene duplications of the filament component ArlB, providing an opportunity to study how gene duplication and neofunctionalization contributed to the radical innovation of rotary function. Toward understanding how this happened, we used electron cryomicroscopy to determine the structure of isolated ArlG filaments, the major component of the stator complex. Using a hybrid modeling approach incorporating structure prediction and validation, we show that ArlG filaments are open helices distinct to the closed helical filaments of ArlB. Curiously, further analysis reveals that ArlG retains a subset of the inter-protomer interactions of homologous ArlB, resulting in a superficially different assembly that nevertheless reflects the common ancestry of the two structures. This relatively simple mechanism to change quaternary structure was likely associated with the evolutionary neofunctionalization of the archaellar stator complex, and we speculate that the relative deformable elasticity of an open helix may facilitate elastic energy storage during the transmission of the discrete bursts of energy released by ATP hydrolysis to continuous archaellar rotation, allowing the inherent properties of a duplicated ArlB to be co-opted to fulfill a new role. Furthermore, agreement of diverse experimental evidence in our work supports recent claims to the power of new structure prediction techniques.Trishant R. UmrekarYvonne B. WinterbornShamphavi SivabalasarmaShamphavi SivabalasarmaJulian BrantlSonja-Verena AlbersSonja-Verena AlbersMorgan BeebyFrontiers Media S.A.articlearchaellar motorstator complexsingle particle analysismolecular evolutionexaptationMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	archaellar motor stator complex single particle analysis molecular evolution exaptation Microbiology QR1-502
spellingShingle	archaellar motor stator complex single particle analysis molecular evolution exaptation Microbiology QR1-502 Trishant R. Umrekar Yvonne B. Winterborn Shamphavi Sivabalasarma Shamphavi Sivabalasarma Julian Brantl Sonja-Verena Albers Sonja-Verena Albers Morgan Beeby Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component
description	Novelty in biology can arise from opportunistic repurposing of nascent characteristics of existing features. Understanding how this process happens at the molecular scale, however, suffers from a lack of case studies. The evolutionary emergence of rotary motors is a particularly clear example of evolution of a new function. The simplest of rotary motors is the archaellum, a molecular motor that spins a helical propeller for archaeal motility analogous to the bacterial flagellum. Curiously, emergence of archaellar rotation may have pivoted on the simple duplication and repurposing of a pre-existing component to produce a stator complex that anchors to the cell superstructure to enable productive rotation of the rotor component. This putative stator complex is composed of ArlF and ArlG, gene duplications of the filament component ArlB, providing an opportunity to study how gene duplication and neofunctionalization contributed to the radical innovation of rotary function. Toward understanding how this happened, we used electron cryomicroscopy to determine the structure of isolated ArlG filaments, the major component of the stator complex. Using a hybrid modeling approach incorporating structure prediction and validation, we show that ArlG filaments are open helices distinct to the closed helical filaments of ArlB. Curiously, further analysis reveals that ArlG retains a subset of the inter-protomer interactions of homologous ArlB, resulting in a superficially different assembly that nevertheless reflects the common ancestry of the two structures. This relatively simple mechanism to change quaternary structure was likely associated with the evolutionary neofunctionalization of the archaellar stator complex, and we speculate that the relative deformable elasticity of an open helix may facilitate elastic energy storage during the transmission of the discrete bursts of energy released by ATP hydrolysis to continuous archaellar rotation, allowing the inherent properties of a duplicated ArlB to be co-opted to fulfill a new role. Furthermore, agreement of diverse experimental evidence in our work supports recent claims to the power of new structure prediction techniques.
format	article
author	Trishant R. Umrekar Yvonne B. Winterborn Shamphavi Sivabalasarma Shamphavi Sivabalasarma Julian Brantl Sonja-Verena Albers Sonja-Verena Albers Morgan Beeby
author_facet	Trishant R. Umrekar Yvonne B. Winterborn Shamphavi Sivabalasarma Shamphavi Sivabalasarma Julian Brantl Sonja-Verena Albers Sonja-Verena Albers Morgan Beeby
author_sort	Trishant R. Umrekar
title	Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component
title_short	Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component
title_full	Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component
title_fullStr	Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component
title_full_unstemmed	Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component
title_sort	evolution of archaellum rotation involved invention of a stator complex by duplicating and modifying a core component
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/a5938ca9cac74d69a5b262583537543f
work_keys_str_mv	AT trishantrumrekar evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT yvonnebwinterborn evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT shamphavisivabalasarma evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT shamphavisivabalasarma evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT julianbrantl evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT sonjaverenaalbers evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT sonjaverenaalbers evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent AT morganbeeby evolutionofarchaellumrotationinvolvedinventionofastatorcomplexbyduplicatingandmodifyingacorecomponent
_version_	1718405077722464256

Evolution of Archaellum Rotation Involved Invention of a Stator Complex by Duplicating and Modifying a Core Component

Ejemplares similares