Collective magnetotaxis of microbial holobionts is optimized by the three-dimensional organization and magnetic properties of ectosymbionts.
Collective magnetotaxis of microbial holobionts is optimized by the three-dimensional organization and magnetic properties of ectosymbionts.
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DOI：
10.1073/pnas.2216975120
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发表时间：
2023-03-07
影响因子：
11.1
通讯作者：
Lefevre, Christopher T.
中科院分区：
文献类型：
--
作者：
Chevrier, Daniel M.;Juhin, Amelie;Menguy, Nicolas;Bolzoni, Romain;Soto-Rodriguez, Paul E. D.;Kojadinovic-Sirinelli, Mila;Paterson, Greig A.;Belkhou, Rachid;Williams, Wyn;Skouri-Panet, Feriel;Kosta, Artemis;Le Guenno, Hugo;Pereiro, Eva;Faivre, Damien;Benzerara, Karim;Monteil, Caroline L.;Lefevre, Christopher T.
最近发现了一个能动的微真核宿主和几十个非能动的、表面附着的磁性细菌共生体之间的共生关系，其中宿主获得地磁场引导的导航，这要归功于细菌产生的亚铁磁性纳米颗粒链（在称为磁小体的细胞器内）。我们的研究结果揭示了每个磁小体链的磁偶极子一致地排列并有效地赋予宿主大的磁矩。值得注意的是，计算出的磁矩大大超过了获得趋磁优势所需的磁矩。这些结果不仅显示了由于细菌的三维组织和磁性，在进化过程中集体趋磁性的优化，而且还提出了关于磁小体功能超出磁场指导的问题，因为它们大量覆盖宿主。在过去的几十年里，共生和全共生体（一个拥有共生体种群的宿主实体）的概念在我们对生命功能和多样性的理解中扮演了核心角色。无论合作伙伴的相互作用的类型，了解如何的生物物理特性的每个单独的共生体和他们的组装可能会产生集体行为的holobiont规模仍然是一个根本的挑战。这在新发现的趋磁全生物（MHB）的情况下特别有趣，MHB的运动依赖于集体趋磁性（即，由化学趋氧性系统引导的磁场辅助运动性）。这种复杂的行为提出了许多关于共生体的磁性如何决定全生物的磁性和运动性的问题。在这里，一套基于光，电子和X射线的显微镜技术[包括X射线磁性圆二色性（XMCD）]揭示了共生体优化了MHB从微米级到纳米级的运动性，超微结构和磁性。在这些磁性共生体的情况下，转移到宿主细胞的磁矩是过量的（比自由生活的趋磁细菌强102至103倍），远高于宿主细胞获得趋磁优势的阈值。共生体的表面组织在本文中明确提出，描绘了确保细胞纵向排列的细菌膜结构。磁小体的磁偶极子和纳米晶取向也被证明是一致的纵向方向，最大限度地提高每个共生体的磁矩。由于宿主细胞具有过多的磁矩，磁小体生物矿化所提供的超出趋磁性的益处可能受到质疑。
Symbiosis between a motile microeukaryotic host and dozens of nonmotile, surface-attached magnetic bacterial symbionts was recently discovered, where the host acquires geomagnetic field-guided navigation thanks to chains of ferrimagnetic nanoparticles (within organelles called magnetosomes) produced by the bacteria. Our findings reveal magnetic dipoles of each magnetosome chain consistently align and efficiently confer a large magnetic moment to the host. Remarkably, the calculated magnetic moment is greatly in excess of that required to gain a magnetotactic advantage. These results not only show an optimization of collective magnetotaxis during the course of evolution owing to the three-dimensional organization and magnetic properties of bacteria but also raise the question on the magnetosome’s function beyond magnetic field guidance since they abundantly cover the host. 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.
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影响因子：
5.1
作者：
Decelle, Johan;Veronesi, Giulia;Musat, Niculina
通讯作者：
Musat, Niculina
影响因子：
2.5
作者：
Belkhou, Rachid;Stanescu, Stefan;Dalle, Didier
通讯作者：
Dalle, Didier
DOI：
10.1002/2017gc007279
发表时间：
2018-04
期刊：
Geochemistry, geophysics, geosystems : G(3)
影响因子：
--
作者：
Ó Conbhuí P;Williams W;Fabian K;Ridley P;Nagy L;Muxworthy AR
通讯作者：
Muxworthy AR
影响因子：
11
作者：
Edgcom, V. P.;Breglia, S. A.;Bernhard, J. M.
通讯作者：
Bernhard, J. M.
影响因子：
9.8
作者：
Belevich I;Joensuu M;Kumar D;Vihinen H;Jokitalo E
通讯作者：
Jokitalo E