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

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 (10 2 to 10 3 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.

Primordial magnetotaxis in putative giant paleoproterozoic magnetofossils

“…For a given population of cells forming an organism, the average alignment , where θ is the angle between the field direction and the magnetization of the organism) is a function dependent on the strength of the magnetic torque produced by the chain and the thermal energy of the fluid’s Brownian motion. Some authors ( 36 ) consider that to offer any biological advantage to a magnetotactic organism, . Even in a basic model containing only three particles under a weak magnetic field of 6 μT, the alignment condition is fulfilled in all of our simulations.…”

“…However, they also showed that alignment in sediment pores is much less efficient compared to MT performing magnetotaxis in the water column. As we cannot determine the living environment, we can simply compare the Brownian alignment in a low magnetic field (as stated above) to be as efficient as that of modern MT (e.g., Magnetobacterium bavaricum ) ( 6 ) and magnetotactic holobionts ( 36 ).…”

“…However, a more realistic model should account for the ellipsoidal shape of a magnetotactic organism. The viscous torque of a prolate ellipsoid (whose main axes are a, b, and c) rotating in a uniformly magnetized fluid ( 42 ) can be assimilated to the U-turn motion approach ( 36 , 37 ) to produce a modified model that allowed us to calculate the hypothetical times for giant magnetofossils.…”

Microbes and Sustainable Living: Focus on Electric and Magnetic Fields

“…For example, the idea that symbiotic magnetic sensing as a collaboration between MTB and host adaptations has gained increasing support [105]. In fact, magnetoreceptive bacteria have been found to be capable of transferring their capacities by producing a collective magnetic fieldassisted motility guided by a chemoaerotaxis system in the holobiont [106].…”