Collective magnetotaxis of microbial holobionts is optimized by the three-dimensional organization and magnetic properties of ectosymbionts
Chevrier, Daniel (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)
Juhin, Amélie (Sorbonne Université. Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie)
Menguy, Nicolas (Sorbonne Université. Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie)
Bolzoni, Romain (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)
Soto-Rodriguez, Paul (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)
Kojadinovic-Sirinelli, Mila (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)
Paterson, Greig (University of Liverpool. Department of Earth, Ocean and Ecological Sciences)
Belkhou, Rachid (Synchrotron Soleil)
Williams, Wyn (University of Edinburgh. School of GeoSciences)
Skouri-Panet, Fériel (Sorbonne Université. Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie)
Kosta, Artemis (Centre national de la recherche scientifique. Institut de Microbiologie de la Méditerranée)
Le Guenno, Hugo (Centre national de la recherche scientifique. Institut de Microbiologie de la Méditerranée)
Pereiro, Eva (Laboratori de Llum del Sincrotró ALBA)
Faivre, Damien (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)
Benzerara, Karim (Sorbonne Université. Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie)
Monteil, Caroline (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)
Lefevre, Christopher T. (Aix-Marseille Université. Bioscience and biotechnology institute of Aix-Marseille)

Date:	2023
Abstract:	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.
Grants:	European Commission 797431
Note:	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).
Rights:	Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, i la comunicació pública de l'obra, sempre que no sigui amb finalitats comercials, i sempre que es reconegui l'autoria de l'obra original. No es permet la creació d'obres derivades.
Language:	Anglès
Document:	Article ; recerca ; Versió publicada
Subject:	Collective magnetotaxis ; Symbiosis ; Magnetosomes ; Biomineralization ; Holobiont
Published in:	Proceedings of the National Academy of Sciences of the United States of America, Vol. 120, issue 10 (March 2023) , art. e2216975120, ISSN 1091-6490

DOI: 10.1073/pnas.2216975120
PMID: 36848579

11 p, 3.5 MB

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