Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi

Abstract CanA from Pyrodictium abyssi, the main constituent of the extracellular protein network of this archaeon, forms a hollow-fiber network in the presence of divalent ions. The polymerization of CanA induced by divalent ions is characterized by (at least) two processes with rate constants of 0....

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Main Authors: Claudia E. Munte, Raphael Kreitner, Reinhard Rachel, Karl O. Stetter, Werner Kremer, Hans Robert Kalbitzer
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-13242-6
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author Claudia E. Munte
Raphael Kreitner
Reinhard Rachel
Karl O. Stetter
Werner Kremer
Hans Robert Kalbitzer
author_facet Claudia E. Munte
Raphael Kreitner
Reinhard Rachel
Karl O. Stetter
Werner Kremer
Hans Robert Kalbitzer
author_sort Claudia E. Munte
collection DOAJ
description Abstract CanA from Pyrodictium abyssi, the main constituent of the extracellular protein network of this archaeon, forms a hollow-fiber network in the presence of divalent ions. The polymerization of CanA induced by divalent ions is characterized by (at least) two processes with rate constants of 0.19 and 0.03 ms-1 at 298 K with a critical monomer concentration of 2.48 µM. A non-polymerizing mutant, K1-CanA, was created, and the NMR solution structure could be determined by multidimensional NMR spectroscopy. It mainly consists of β-pleated sheets and 2 small α-helices, arranged as β1β2β3β4α1β5β6α2β7β8β9β10β11β12β13. Of the 13 β-strands, 8 form a non-canonical jellyroll class I fold. Several interaction sites for divalent ions could be identified by [1H, 15N]-SOFAST-HMQC spectroscopy in two main surface areas called BA1 and BA2, located at both ends of the jellyroll. The binding of divalent ions to the monomer induces significant local structural changes in these areas. In general, the affinities for Mg2+-ions to the sites in BA1 are smaller than those for Ca2+-ions. In contrast, in binding area BA2, Mg2+- and Ca2+-affinities are similar. The data suggest a conformational selection mechanism induced by ion binding as a first step in the polymerization process of CanA.
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spelling doaj-art-5da86d9d8dd34fb5a66ffc10a6863d902025-08-20T03:42:39ZengNature PortfolioScientific Reports2045-23222025-08-0115112310.1038/s41598-025-13242-6Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssiClaudia E. Munte0Raphael Kreitner1Reinhard Rachel2Karl O. Stetter3Werner Kremer4Hans Robert Kalbitzer5Institute of Biophysics and Physical Biochemistry, Biophysics I and Centre of Magnetic Resonance in Chemistry and Biomedicine (CMRCB), University of RegensburgInstitute of Biophysics and Physical Biochemistry, Biophysics I and Centre of Magnetic Resonance in Chemistry and Biomedicine (CMRCB), University of RegensburgCentre for Electron Microscopy, University of RegensburgLehrstuhl für Mikrobiologie und Archaeen-Zentrum, University of RegensburgInstitute of Biophysics and Physical Biochemistry, Biophysics I and Centre of Magnetic Resonance in Chemistry and Biomedicine (CMRCB), University of RegensburgInstitute of Biophysics and Physical Biochemistry, Biophysics I and Centre of Magnetic Resonance in Chemistry and Biomedicine (CMRCB), University of RegensburgAbstract CanA from Pyrodictium abyssi, the main constituent of the extracellular protein network of this archaeon, forms a hollow-fiber network in the presence of divalent ions. The polymerization of CanA induced by divalent ions is characterized by (at least) two processes with rate constants of 0.19 and 0.03 ms-1 at 298 K with a critical monomer concentration of 2.48 µM. A non-polymerizing mutant, K1-CanA, was created, and the NMR solution structure could be determined by multidimensional NMR spectroscopy. It mainly consists of β-pleated sheets and 2 small α-helices, arranged as β1β2β3β4α1β5β6α2β7β8β9β10β11β12β13. Of the 13 β-strands, 8 form a non-canonical jellyroll class I fold. Several interaction sites for divalent ions could be identified by [1H, 15N]-SOFAST-HMQC spectroscopy in two main surface areas called BA1 and BA2, located at both ends of the jellyroll. The binding of divalent ions to the monomer induces significant local structural changes in these areas. In general, the affinities for Mg2+-ions to the sites in BA1 are smaller than those for Ca2+-ions. In contrast, in binding area BA2, Mg2+- and Ca2+-affinities are similar. The data suggest a conformational selection mechanism induced by ion binding as a first step in the polymerization process of CanA.https://doi.org/10.1038/s41598-025-13242-6
spellingShingle Claudia E. Munte
Raphael Kreitner
Reinhard Rachel
Karl O. Stetter
Werner Kremer
Hans Robert Kalbitzer
Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi
Scientific Reports
title Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi
title_full Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi
title_fullStr Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi
title_full_unstemmed Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi
title_short Biophysical characterization and solution structure of the cannulae-forming protein CanA from the hyperthermophilic archaeon Pyrodictium abyssi
title_sort biophysical characterization and solution structure of the cannulae forming protein cana from the hyperthermophilic archaeon pyrodictium abyssi
url https://doi.org/10.1038/s41598-025-13242-6
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