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RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)

Amyloids represent protein aggregates with highly ordered fibrillar structure associated with the development of various disorders in humans and animals and involved in implementation of different vital functions in all three domains of life. In prokaryotes, amyloids perform a wide repertoire of fun...

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Autores principales: Kosolapova, Anastasiia O., Belousov, Mikhail V., Sulatsky, Maksim I., Tsyganova, Anna V., Sulatskaya, Anna I., Bobylev, Alexander G., Shtark, Oksana Y., Tsyganov, Viktor E., Volkov, Kirill V., Zhukov, Vladimir A., Tikhonovich, Igor A., Nizhnikov, Anton A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650718/
https://www.ncbi.nlm.nih.gov/pubmed/36388578
http://dx.doi.org/10.3389/fpls.2022.1014699
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author Kosolapova, Anastasiia O.
Belousov, Mikhail V.
Sulatsky, Maksim I.
Tsyganova, Anna V.
Sulatskaya, Anna I.
Bobylev, Alexander G.
Shtark, Oksana Y.
Tsyganov, Viktor E.
Volkov, Kirill V.
Zhukov, Vladimir A.
Tikhonovich, Igor A.
Nizhnikov, Anton A.
author_facet Kosolapova, Anastasiia O.
Belousov, Mikhail V.
Sulatsky, Maksim I.
Tsyganova, Anna V.
Sulatskaya, Anna I.
Bobylev, Alexander G.
Shtark, Oksana Y.
Tsyganov, Viktor E.
Volkov, Kirill V.
Zhukov, Vladimir A.
Tikhonovich, Igor A.
Nizhnikov, Anton A.
author_sort Kosolapova, Anastasiia O.
collection PubMed
description Amyloids represent protein aggregates with highly ordered fibrillar structure associated with the development of various disorders in humans and animals and involved in implementation of different vital functions in all three domains of life. In prokaryotes, amyloids perform a wide repertoire of functions mostly attributed to their interactions with other organisms including interspecies interactions within bacterial communities and host-pathogen interactions. Recently, we demonstrated that free-living cells of Rhizobium leguminosarum, a nitrogen-fixing symbiont of legumes, produce RopA and RopB which form amyloid fibrils at cell surface during the stationary growth phase thus connecting amyloid formation and host-symbiont interactions. Here we focused on a more detailed analysis of the RopB amyloid state in vitro and in vivo, during the symbiotic interaction between R. leguminosarum bv. viciae with its macrosymbiont, garden pea (Pisum sativum L.). We confirmed that RopB is the bona fide amyloid protein since its fibrils exhibit circular x-ray reflections indicating its cross-β structure specific for amyloids. We found that fibrils containing RopB and exhibiting amyloid properties are formed in vivo at the surface of bacteroids of R. leguminosarum extracted from pea nodules. Moreover, using pea sym31 mutant we demonstrated that formation of extracellular RopB amyloid state occurs at different stages of bacteroid development but is enhanced in juvenile symbiosomes. Proteomic screening of potentially amyloidogenic proteins in the nodules revealed the presence of detergent-resistant aggregates of different plant and bacterial proteins including pea amyloid vicilin. We demonstrated that preformed vicilin amyloids can cross-seed RopB amyloid formation suggesting for probable interaction between bacterial and plant amyloidogenic proteins in the nodules. Taken together, we demonstrate that R. leguminosarum bacteroids produce extracellular RopB amyloids in pea nodules in vivo and these nodules also contain aggregates of pea vicilin amyloid protein, which is able to cross-seed RopB fibrillogenesis in vitro. Thus, we hypothesize that plant nodules contain a complex amyloid network consisting of plant and bacterial amyloids and probably modulating host-symbiont interactions.
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spelling pubmed-96507182022-11-15 RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.) Kosolapova, Anastasiia O. Belousov, Mikhail V. Sulatsky, Maksim I. Tsyganova, Anna V. Sulatskaya, Anna I. Bobylev, Alexander G. Shtark, Oksana Y. Tsyganov, Viktor E. Volkov, Kirill V. Zhukov, Vladimir A. Tikhonovich, Igor A. Nizhnikov, Anton A. Front Plant Sci Plant Science Amyloids represent protein aggregates with highly ordered fibrillar structure associated with the development of various disorders in humans and animals and involved in implementation of different vital functions in all three domains of life. In prokaryotes, amyloids perform a wide repertoire of functions mostly attributed to their interactions with other organisms including interspecies interactions within bacterial communities and host-pathogen interactions. Recently, we demonstrated that free-living cells of Rhizobium leguminosarum, a nitrogen-fixing symbiont of legumes, produce RopA and RopB which form amyloid fibrils at cell surface during the stationary growth phase thus connecting amyloid formation and host-symbiont interactions. Here we focused on a more detailed analysis of the RopB amyloid state in vitro and in vivo, during the symbiotic interaction between R. leguminosarum bv. viciae with its macrosymbiont, garden pea (Pisum sativum L.). We confirmed that RopB is the bona fide amyloid protein since its fibrils exhibit circular x-ray reflections indicating its cross-β structure specific for amyloids. We found that fibrils containing RopB and exhibiting amyloid properties are formed in vivo at the surface of bacteroids of R. leguminosarum extracted from pea nodules. Moreover, using pea sym31 mutant we demonstrated that formation of extracellular RopB amyloid state occurs at different stages of bacteroid development but is enhanced in juvenile symbiosomes. Proteomic screening of potentially amyloidogenic proteins in the nodules revealed the presence of detergent-resistant aggregates of different plant and bacterial proteins including pea amyloid vicilin. We demonstrated that preformed vicilin amyloids can cross-seed RopB amyloid formation suggesting for probable interaction between bacterial and plant amyloidogenic proteins in the nodules. Taken together, we demonstrate that R. leguminosarum bacteroids produce extracellular RopB amyloids in pea nodules in vivo and these nodules also contain aggregates of pea vicilin amyloid protein, which is able to cross-seed RopB fibrillogenesis in vitro. Thus, we hypothesize that plant nodules contain a complex amyloid network consisting of plant and bacterial amyloids and probably modulating host-symbiont interactions. Frontiers Media S.A. 2022-10-24 /pmc/articles/PMC9650718/ /pubmed/36388578 http://dx.doi.org/10.3389/fpls.2022.1014699 Text en Copyright © 2022 Kosolapova, Belousov, Sulatsky, Tsyganova, Sulatskaya, Bobylev, Shtark, Tsyganov, Volkov, Zhukov, Tikhonovich and Nizhnikov https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Kosolapova, Anastasiia O.
Belousov, Mikhail V.
Sulatsky, Maksim I.
Tsyganova, Anna V.
Sulatskaya, Anna I.
Bobylev, Alexander G.
Shtark, Oksana Y.
Tsyganov, Viktor E.
Volkov, Kirill V.
Zhukov, Vladimir A.
Tikhonovich, Igor A.
Nizhnikov, Anton A.
RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)
title RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)
title_full RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)
title_fullStr RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)
title_full_unstemmed RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)
title_short RopB protein of Rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (Pisum sativum L.)
title_sort ropb protein of rhizobium leguminosarum bv. viciae adopts amyloid state during symbiotic interactions with pea (pisum sativum l.)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650718/
https://www.ncbi.nlm.nih.gov/pubmed/36388578
http://dx.doi.org/10.3389/fpls.2022.1014699
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