Collective magnetotaxis of microbial holobionts is optimized by the three-dimensional organization and magnetic properties of ectosymbionts

Autor: Daniel M. Chevrier, Amélie Juhin, Nicolas Menguy, Romain Bolzoni, Paul E. D. Soto-Rodriguez, Mila Kojadinovic-Sirinelli, Greig A. Paterson, Rachid Belkhou, Wyn Williams, Fériel Skouri-Panet, Artemis Kosta, Hugo Le Guenno, Eva Pereiro, Damien Faivre, Karim Benzerara, Caroline L. Monteil, Christopher T. Lefevre
Přispěvatelé: Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB) (BIAM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Cosmochimie [IMPMC] (IMPMC_COSMO), Institut de minéralogie, de physique des matériaux et de cosmochimie (IMPMC), Muséum national d'Histoire naturelle (MNHN)-Institut de recherche pour le développement [IRD] : UR206-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Muséum national d'Histoire naturelle (MNHN)-Institut de recherche pour le développement [IRD] : UR206-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Department of Earth Ocean and Ecological Sciences [Liverpool], University of Liverpool, Synchrotron SOLEIL (SSOLEIL), Centre National de la Recherche Scientifique (CNRS), School of Geosciences [Edinburgh], University of Edinburgh, Institut de Microbiologie de la Méditerranée (IMM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), ALBA Synchrotron light source [Barcelone], ANR-21-CE02-0034,SymbioMAGNET,ETUDE DE LA BIODIVERSITE, DE L'ECOLOGIE ET DE L'EVOLUTION DE LA SYMBIOSE MAGNETOTACTIQUE(2021), European Project: 797431,BioNanoMagnets
Jazyk: angličtina
Rok vydání: 2023
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences of the United States of America, 2023, 120 (10), pp.e2216975120. ⟨10.1073/pnas.2216975120⟩
Chevrier, D M, Juhin, A, Menguy, N, Bolzoni, R, Soto-Rodriguez, P E D, Kojadinovic-Sirinelli, M, Paterson, G A, Belkhou, R, Williams, W, Skouri-Panet, F, Kosta, A, Le guenno, H, Pereiro, E, Faivre, D, Benzerara, K, Monteil, C L & Lefevre, C T 2023, ' Collective magnetotaxis of microbial holobionts is optimized by the three-dimensional organization and magnetic properties of ectosymbionts ', Proceedings of the National Academy of Sciences (PNAS), vol. 120, no. 10, e2216975120 . https://doi.org/10.1073/pnas.2216975120
ISSN: 0027-8424
1091-6490
DOI: 10.1073/pnas.2216975120⟩
Popis: Altres ajuts: D.M.C. and D.F. acknowledge awarded ALBA synchrotron beamtimes (Proposals 2018022677 and 2019023346), Mistral beamline staff for assistance in cryo-SXT experiments and CALIPSOplus funding for Proposal 2019023346. We acknowledge Soleil Synchrotron for beamtime awarded (Proposal 20191124) for experiments on the Hermes beamline (STXM-XMCD). Over the last few decades, symbiosis and the concept of holobiont-a host entity with a population of symbionts-have gained a central role in our understanding of life functioning and diversification. Regardless of the type of partner interactions, understanding how the biophysical properties of each individual symbiont and their assembly may generate collective behaviors at the holobiont scale remains a fundamental challenge. This is particularly intriguing in the case of the newly discovered magnetotactic holobionts (MHB) whose motility relies on a collective magnetotaxis (i.e., a magnetic field-assisted motility guided by a chemoaerotaxis system). This complex behavior raises many questions regarding how magnetic properties of symbionts determine holobiont magnetism and motility. Here, a suite of light-, electron- and X-ray-based microscopy techniques [including X-ray magnetic circular dichroism (XMCD)] reveals that symbionts optimize the motility, the ultrastructure, and the magnetic properties of MHBs from the microscale to the nanoscale. In the case of these magnetic symbionts, the magnetic moment transferred to the host cell is in excess (102 to 103 times stronger than free-living magnetotactic bacteria), well above the threshold for the host cell to gain a magnetotactic advantage. The surface organization of symbionts is explicitly presented herein, depicting bacterial membrane structures that ensure longitudinal alignment of cells. Magnetic dipole and nanocrystalline orientations of magnetosomes were also shown to be consistently oriented in the longitudinal direction, maximizing the magnetic moment of each symbiont. With an excessive magnetic moment given to the host cell, the benefit provided by magnetosome biomineralization beyond magnetotaxis can be questioned.
Databáze: OpenAIRE
Externí odkaz: