Three magnetotactic bacteria, designated strains PR-1T, PR-2T and PR-3T, were isolated from seawater collected from the Mediterranean Sea at the Pointe Rouge Marina in Marseille, France. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain PR-1T formed a clade with representatives of the genus Terasakiella, which previously did not include any magnetotactic members. Strains PR-1T shared 97.90% sequence similarity with Terasakiella brassicae B3T. Strains PR-2T and PR-3T were closely related to previously known magnetotactic strains, Magnetovibrio blakemorei MV-1T and Magnetococcus marinus MC-1T, with 16S rRNA gene sequence similarity of 94.40% and 97.39%, respectively. Strain PR-1T is a spirillum that produces two single flagella at each pole; strain PR-2T is a vibrio equipped with a single polar flagellum, while strain PR-3T is roughly spherical, with two sheathed bundles of flagella at a single pole (bilophotrichous). The major cellular fatty acids are C18 : 1 ω7c and C16 : 1 ω7c for strain PR-1T; C18 : 1 ω7c, C16 : 1 ω7c and C16 : 0 for strain PR-2T; and C16 : 1 ω7c and C16 : 0 for strain PR-3T. Based on phenotypic, genotypic and phylogenetic data, all three strains, PR-1T, PR-2T and PR-3T, are considered to represent three novel species. Strain PR-1T belongs to the genus Terasakiella, for which the name Terasakiella magnetica sp. nov. is proposed. The type strain is PR-1T (=TSD-367T=JCM 39464T). Strain PR-2T belongs to the genus Magnetovibrio, for which the name Magnetovibrio massiliensis sp. nov. is proposed. The type strain is PR-2T (=TSD-368T=JCM 39465T). Strain PR-3T belongs to the genus Magnetococcus, for which the name Magnetococcus organivorans sp. nov. is proposed. The type strain is PR-3T (=TSD-369T=JCM 39466T).

Magnetoreception is a remarkable ability found across a diverse range of organisms, including bacteria, birds, fish, insects, and mammals, enabling them to detect and harness the Earth's geomagnetic field. Recently, the recruitment of biomineralizing ectosymbionts by euglenozoans was evidenced as an ecological strategy for microeukaryotes to acquire this sense. Here, we report a case of magnetosymbiosis involving a ciliate and four populations of endosymbiotic bacteria experiencing genome reduction. Among these bacteria, one group of sulphate-reducing Desulfovibrionales was found to biomineralize bundles of bullet-shaped magnetite crystals. The ciliate's magnetotaxis mirrors that of free-living magnetotactic bacteria and euglenozoans, enabling efficient navigation in chemically stratified aquatic environments. However, in this case, magnetotaxis arises from an endosymbiotic interaction. Using a combination of optical-, confocal-, electron- and X-ray-based microscopy techniques, together with genomic analyses, these findings demonstrate that magnetosymbiosis can emerge in unicellular eukaryotic lineages through endosymbiotic integration, expanding our understanding of such interactions in aquatic ecosystems. More broadly, this work contributes to the ongoing debate on the origins of magnetoreception in eukaryotes.

Some bacteria genetically control the biomineralisation of intracellular amorphous calcium carbonates (iACC) with potential implications for microbial physiology, evolution, bioremediation and biogeochemical cycling. Until now, this capacity has been documented in Cyanobacteria, the giant gammaproteobacterium Achromatium and a few magnetotactic Pseudomonadota and Nitrospirota. Here, we report the discovery of iACC biomineralisation in members of the Methylococcaceae, a family of aerobic methanotrophic Gammaproteobacteria. A homologue of the ccyA gene, a diagnostic marker for iACC formation in Cyanobacteria, was identified in several Methylococcaceae genomes, based on the conserved C-terminal (GlyZip)3 domain of the encoded calcyanin protein. Moreover, two cultivated strains, Methylococcus geothermalis and Methylococcus mesophilus, whose genomes contained the ccyA gene, were consistently shown to form iACC. The ccyA genes of Methylococcaceae and Microcystis share higher sequence similarity than with other Cyanobacteria, suggesting horizontal gene transfer (HGT) from an ancestral Microcystis-like cyanobacterium to Methylococcaceae. This finding extends the known taxonomic distribution of ccyA and suggests that the capability to biomineralize iACC was acquired by HGT. The discovery of iACC in methane-oxidising Methylococcaceae highlights a previously unrecognised coupling between calcium carbonate biomineralisation and methane cycling in aquatic environments, suggesting an overlooked role of iACC formation in microbial carbon storage and local geochemical regulation.

Magnetotactic bacteria form a highly diverse group of microorganisms, yet early exploration of their diversity was largely centered on the Pseudomonadota. More recently, metagenomic studies have revealed that magnetotaxis, a form of chemotaxis guided by Earth's magnetic field, is widespread in other deep-branching phyla for which little to no ecological or biological information is available beyond that inferred from their genomes. For most of them, the morphology, ultrastructure and magnetosome chain characteristics responsible for the magnetic guidance remain unknown. While screening extreme environments for novel magnetotactic species, we observed magnetotactic Bdellovibrionota in the anoxic and ferruginous sediments of the Fontaine Goyon spring (France). We characterized their cell morphology and ultrastructure using magnetic enrichment, a single-cell sorting approach, and high-resolution electron microscopy. Cells display the morphology typical of the few predatory bacteria described in this phylum, and biomineralize, on average, five irregularly faceted, bullet-shaped magnetite magnetosomes along the concave side of the cell. Metagenomic analysis of approximately 100 cells revealed a potentially predatory and heterotrophic lifestyle adapted to low-O2 conditions. It also suggests a flexible respiratory metabolism under varying redox conditions, using iron as an alternative terminal electron acceptor. Exploring the diversity of Bdellovibrionota in public databases, we found 21 metagenome-assembled-genomes containing magnetosome genes. None of them harbor the canonical mamK actin-like gene implicated in aligning magnetosomes in described magnetotactic models. Affiliated to an undescribed class, we propose a classification scheme for the magnetotactic Bdellovibrionota species representing the class Bdellonasia class nov., for which no species had been formally described.

Abstract The coexistence of chirality and magnetism in nanomaterials has been observed with metallic complexes but remains rarely achieved in magnetic oxides. Here, we identify biologically induced chiroptical activity in the magnetotactic bacterium Magnetospirillum gryphiswaldense strain MSR-1, which biomineralizes Fe3O4 crystals within a prokaryotic organelle known as a magnetosome. Natural and magnetic circular dichroism spectra were recorded for wild-type MSR-1, a magnetosome-deficient mutant (ΔmamAB), and the magnetosomes extracted from the bacterial cells. While chiroptical signals appeared when the particles remained within the bacterial matrix, the isolated nanoparticles did not demonstrate detectable natural optical activity. Subsequent surface modification of the extracted optically inactive nanoparticles with enantiopure aspartic acid produced chiroptical responses. These observations suggest that the biological environment of magnetosomes imposes chiral asymmetry on magnetic nanoparticles and that surface functionalization revealed optical activity. The results collectively describe a biologically mediated induction of chiroptical signals in Fe3O4 nanoparticles.

Multicellular magnetotactic prokaryotes represent a unique group of obligately marine multicellular bacteria known for their ability to navigate along magnetic field lines thanks to ferrimagnetic nanocrystals. To date, two distinct spherical and ellipsoidal morphotypes have been described, typically ranging from 3 to 6 μm in diameter and comprising approximately 50 cells of the same species. Although widespread in highly reduced marine sediments, they are represented by solely three genera clustering into a monophyletic group within the Desulfobacterota. In this study, we report a third morphotype in reduced sediments of the Mediterranean Sea in Carry-le-Rouet, France, i.e. approximately 30 times more voluminous than any previously described form. Because their large size, we designated these multicellular bacteria as "giant" and explored their cell ultrastructure, ecological niche and physiology using magnetic enrichment and a combination of microscopy techniques and single-consortium genomics. Transmission electron microscopy and confocal microscopy images of several individual consortia revealed that they contain an average of 130 cells, each producing over 100 greigite magnetosomes arranged to optimize the overall magnetic moment. Phylogenomic analyses positioned giant multicellular magnetotactic prokaryotes, together with other morphotypes, in a previously undescribed genus and species within the Candidatus Magnetomoraceae family, named Magnetogigantoglobus mediterraneus. Although genetically divergent with a different ultrastructure, all multicellular magnetotactic prokaryotes seem to rely on sulfate reduction coupled to heterotrophy or autotrophy. We further discuss the significance of these findings in the context of the evolutionary history of multicellularity and magnetotaxis in prokaryotes.

A magnetotactic bacterium, designated strain SS-5T, was isolated from the Salton Sea, a highly saline lake in California, USA, and cultivated in axenic culture. The Gram-negative cells of strain SS-5T are relatively small and rod-shaped and possess a single polar flagellum (monotrichous). This strain is a magnetotactic bacterium producing magnetite nanocrystals aligned in one chain per cell. Strain SS-5T is a microaerophile that grows chemolithoautotrophically while reducing oxygen as a terminal electron acceptor. Optimal growth occurred at pH 7.0-7.3 and 28-36 °C with thiosulfate used as an electron donor and sodium bicarbonate as a carbon source. Based on its genome sequence, the G + C content is 61.6 %. Phylogenomic and phylogenetic analyses indicate that strain SS-5T belongs to the Sedimenticolaceae family within the Gammaproteobacteria class. Based on average amino acid identity, strain SS-5T can be considered as a novel species of a new genus, for which the name Magnetovirga frankeli is proposed. The type strain of M. frankeli is SS-5T (=DSM 116211T = JCM 39467T).

Intracellular calcium carbonate formation has long been associated with a single genus of giant Gammaproteobacteria, Achromatium. However, this biomineralization has recently received increasing attention after being observed in photosynthetic Cyanobacteriota and in two families of magnetotactic bacteria affiliated with the Alphaproteobacteria. In the latter group, bacteria form not only intracellular amorphous calcium carbonates into large inclusions that are refringent under the light microscope, but also intracellular ferrimagnetic crystals into organelles called magnetosomes. Here new observations suggest that magnetotactic bacteria previously identified in the sediments and water column of Lake Pavin (France) were only a small fraction of the diversity of bacteria producing intracellular amorphous calcium carbonates. To explore this diversity further, we conducted a comprehensive investigation of magnetotactic populations with refractive granules using a combination of environmental microbiology, genomic and mineralogy approaches on cells sorted by micromanipulation. Several species belonging to divergent genera of two Pseudomonadota classes were identified and characterized. Scanning transmission electron microscopy coupled with energy-dispersive X-ray spectrometry support that all these species indeed form intracellular amorphous calcium carbonates. Cryo soft X-ray tomography experiments conducted on ice-vitrified cells, enabled 3D investigation of inclusions volume, which was found to occupy 44-68% of the cell volume. Metabolic network modeling highlighted different metabolic abilities of Alpha- and Gammaproteobacteria, including methylotrophy and CO2 fixation via the reverse Krebs cycle or the Calvin-Benson-Bassham cycle. Overall, this study strengthens a convergent evolution scenario for intracellular carbonatogenesis in Bacteria, and further supports that it is promoted by the fixation of CO2 in anoxic environments.

Magnetotactic bacteria (MTB) possess the ability to precipitate intracellular nanosized magnetite. Their emergence may date back to the early Archean (e.g. 3 Ga) but evidence of such a long history has yet to be provided. MTB identification in the rock record relies on magnetofossils, the residual magnetite crystals that may survive in time to rock deformation and low-grade metamorphism. Several criteria such as size, shape and magnetic properties have been proposed to distinguish magnetofossils from other magnetite sources. Recent experimental work on the freshwater strain Magnetospirillum magneticum AMB-1 revealed that Fe isotope composition represents a promising additional criterion, but isotopic characterization of distinct MTB strains and of their magnetite needs to be provided to evaluate the robustness of iron isotope signatures for paleontological applications. In the present work, we investigate the marine strain Magnetovibrio blakemorei MV-1 under various conditions selected to examine the influence of Fe concentration (50, 100 and 150 mu M) and redox state (Fe(II)-ascorbate or Fe(III)citrate) on bacterial biomineralization and determine associated Fe isotope fractionations. Our results confirm the preferential incorporation of light iron isotopes into magnetite relative to the bacterial growth medium previously observed in AMB-1. Modeling the evolution of the growth medium and magnetite isotope compositions by Rayleigh distillation process yields iron isotope fractionations (i.e. Delta 56Fegrowth medium-magnetite = delta 56Fegrowth medium-delta 56Femagnetite) ranging between 0.2 and 0.9 %o with a mean value of 0.55 (+/- 0.35) %o. This isotope fractionation shows no clear relation with iron concentration or redox state. Importantly, the enrichment in light iron isotope of biological magnetite contrasts with the isotopic characteristics of magnetite formed by abiotic precipitation, the latter being enriched in heavy isotopes. This suggests that Fe isotopes could be used as a biosignature for magnetofossils identification in terrestrial or extraterrestrial samples. Finally, in contrast with previous results obtained on AMB-1, no specific enrichment of 57Fe (relative to 54Fe, 56Fe and 58Fe) could be detected in MV-1 magnetite, which we interpret by differences in iron budgets between the two strains.

Magnetosensitive organisms have the ability to sense and respond actively to features of magnetic fields such as the direction or magnitude. Until now, magnetosensing has been characterized primarily in higher organisms, involving either a cryptochrome-based mechanism or direct magnetic interactions with magnetic particles. Magnetotactic bacteria, microorganisms forming intracellular chains of magnetic nanoparticles, are thought to only passively orient along field lines. In this study, we reveal that the cultivated magnetotactic bacterium SS-5 also exhibits magnetosensing. The microorganisms indeed swim faster in a physiological magnetic field compared to when the field is canceled. This speed difference is independent of illumination wavelength but is altered when the bacterial magnetic backbone is disrupted. We thus propose that magnetosensing in the bacteria originates from a magnetomechanical signal transduction along the magnetotactic filament. Our findings also show that this response depends on relative changes in magnetic field intensity, akin to the Weber-Fechner laws, suggesting that magnetosensing operates similarly to other forms of taxes.

Abstract Intracellular calcium carbonate formation has long been associated with a single genus of giant Gammaproteobacteria, Achromatium. However, this biomineralization has recently received increasing attention after being observed in photosynthetic Cyanobacteriota and in two families of magnetotactic bacteria affiliated with the Alphaproteobacteria. In the latter group, bacteria form not only intracellular amorphous calcium carbonates into large inclusions that are refringent under the light microscope, but also intracellular ferrimagnetic crystals into organelles called magnetosomes. Here new observations suggest that magnetotactic bacteria previously identified in the sediments and water column of Lake Pavin (France) were only a small fraction of the diversity of bacteria producing intracellular amorphous calcium carbonates. To explore this diversity further, we conducted a comprehensive investigation of magnetotactic populations with refractive granules using a combination of environmental microbiology, genomic and mineralogy approaches on cells sorted by micromanipulation. Several species belonging to divergent genera of two Pseudomonadota classes were identified and characterized. Scanning transmission electron microscopy coupled with energy-dispersive X-ray spectrometry support that all these species indeed form intracellular amorphous calcium carbonates. Cryo soft X-ray tomography experiments conducted on ice-vitrified cells, enabled 3D investigation of inclusions volume, which was found to occupy 44 – 68% of the cell volume. Metabolic network modeling highlighted different metabolic abilities of Alpha- and Gammaproteobacteria, including methylotrophy and CO2 fixation via the reverse Krebs cycle or the Calvin-Benson-Bassham cycle. Overall, this study strengthens a convergent evolution scenario for intracellular carbonatogenesis in Bacteria, and further supports that it is promoted by the fixation of CO2 in anoxic environments.

Magnetotactic bacteria (MTB) produce intracellular magnetite (Fe3O4) nanoparticles in a genetically controlled manner. They may represent some of the oldest biomineralizing organisms available in the geological record, but identification of their fossils remains highly debated. While organic molecules are degraded during diagenesis and metamorphic processes, MTB magnetite nanocrystals can be efficiently preserved in the rock record and are referred to as magnetofossils. Experimental work on the freshwater bacterium Magnetospirillum magneticum strain AMB-1 has demonstrated specific minor and trace element patterns distinct from those of abiotic magnetite, and were proposed as a tool for magnetofossil identification. These promising geochemical signatures need to be validated in diverse MTB strains to be used for paleontological reconstruction. Here, we cultivated a marine MTB (Magnetovibrio blakemorei strain MV-1) under various chemical conditions to test possible generalization of this new proxy. MV-1 was grown under various Fe concentrations (50, 100 and 150 mu M) and redox states using either Fe(II)-ascorbate or Fe(III)-citrate as Fe sources. The chemical compositions of the growth media and extracted magnetite crystals were determined by ICP-MS analyses to quantify the partitioning of trace and minor elements between magnetite and solution. Results show that partition coefficients do not depend at first order on the Fe concentration and redox state, a crucial conclusion for potential application to natural systems. A comparison of the two strains shows that MV-1 magnetite generally contains higher concentrations of impurities than AMB-1 magnetite. However, a number of elements possess similar partition coefficients and may represent useful chemical proxies for testing the biological origin of magnetite. These consistent elements can be separated into three groups. The first group is composed of elements (Co, Mn, Pb, Sr) highly depleted in MTB magnetite relative to abiotic magnetite. The second group contains elements with similar partitioning in MTB and abiotic magnetite, including Ca and Li. This group may serve as a reference for constraining a paleo-fluid composition. The last group contains elements (Mo, Sn, Se) enriched in MTB magnetite relative to abiotic magnetite. Such enrichments might be related to biological function of those elements. Chemical patterns determined from laboratory experiments therefore represent promising chemical proxies to identify MTB magnetite in the rock record but now need to be tested in modern natural environments, where MTB and surrounding solution can be jointly collected.

Magnetotactic bacteria have been the only known magnetoreceptive microorganisms for decades. Even if the existence of magnetotactic protists was suggested in 1986, this is only 30 years later that magnetotaxis was extended to the domain of Eukaryota, thanks to the characterization of magnetotactic symbiotic assemblies composed of a flagellated protist and bacteria biomineralizing magnetic crystals. Their mutualistic ectosymbiosis relies on a collective magnetotaxis coupled to a hydrogen-based syntrophy. This new form of cooperation challenges our view of magnetic biomineralization in prokaryotes and magnetoreception in eukaryotes. In this review, we present how magnetosymbiosis was discovered and how cooperation functions. Finally, we discuss the future research and the new perspectives such discovery brought to the field of magnetotaxis.

Abstract Cells of magnetotactic bacteria are used as model systems for studying the magnetic properties of ferrimagnetic nanocrystals. Each individual bacterial strain produces magnetosomes (membrane-bounded magnetic crystals) that have distinct sizes, shapes, crystallographic orientations and spatial arrangements, thereby providing nanoparticle systems whose unique magnetic properties are unmatched by synthetic chemically-produced crystals. Here, we use off-axis electron holography in the transmission electron microscope to study the magnetic properties of isolated and closely-spaced bullet-shaped magnetite (Fe3O4) magnetosomes biomineralized by the following magnetotactic bacterial strains: the cultured Desulfovibrio magneticus RS-1 and the uncultured strains LO-1 and HSMV-1. These bacteria biomineralize magnetite crystals whose crystallographic axes of elongation are parallel to <100> (RS-1 and LO-1) or <110> (HSMV-1). We show that the individual magnetosome crystals are single magnetic domains and measure their projected in-plane magnetization distributions and magnetic dipole moments. We use analytical modelling to assess the interplay between shape anisotropy and the magnetically preferred <111> magneto-crystalline easy axis of magnetite.

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 (102to 103times 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.

Magnetosomes of magnetotactic bacteria (MTB) consist of structurally perfect, nano-sized magnetic crystals enclosed within vesicles of a proteo-lipid membrane. In species of Magnetospirillum, biosynthesis of their cubo-octahedral-shaped magnetosomes was recently demonstrated to be a complex process, governed by about 30 specific genes that are comprised within compact magnetosome gene clusters (MGCs). Similar, yet distinct gene clusters were also identified in diverse MTB that biomineralize magnetosome crystals with different, genetically encoded morphologies. However, since most representatives of these groups are inaccessible by genetic and biochemical approaches, their analysis will require the functional expression of magnetosome genes in foreign hosts. Here, we studied whether conserved essential magnetosome genes from closely and remotely related MTB can be functionally expressed by rescue of their respective mutants in the tractable model Magnetospirillum gryphiswaldense of the Alphaproteobacteria. Upon chromosomal integration, single orthologues from other magnetotactic Alphaproteobacteria restored magnetosome biosynthesis to different degrees, while orthologues from distantly related Magnetococcia and Deltaproteobacteria were found to be expressed but failed to re-induce magnetosome biosynthesis, possibly due to poor interaction with their cognate partners within multiprotein magnetosome organelle of the host. Indeed, co-expression of the known interactors MamB and MamM from the alphaproteobacterium Magnetovibrio blakemorei increased functional complementation. Furthermore, a compact and portable version of the entire MGCs of M. magneticum was assembled by transformation-associated recombination cloning, and it restored the ability to biomineralize magnetite both in deletion mutants of the native donor and M. gryphiswaldense, while co-expression of gene clusters from both M. gryphiswaldense and M. magneticum resulted in overproduction of magnetosomes. IMPORTANCE We provide proof of principle that Magnetospirillum gryphiswaldense is a suitable surrogate host for the functional expression of foreign magnetosome genes and extended the transformation-associated recombination cloning platform for the assembly of entire large magnetosome gene cluster, which could then be transplanted to different magnetotactic bacteria. The reconstruction, transfer, and analysis of gene sets or entire magnetosome clusters will be also promising for engineering the biomineralization of magnetite crystals with different morphologies that would be valuable for biotechnical applications.

Some organisms have the unique capacity to geolocate and navigate in response to the Earth’s magnetic field lines. Migratory birds and fishes are the best-documented animals that evolved this capacity to guide their movements. In the microbial world, magnetotactic bacteria (MTB) and multicellular magnetotactic prokaryotes (MMPs) have been the only known magnetoreceptive microorganisms for decades. Some microeukaryotes also orient their motility axis along magnetic field lines thanks to the exploitation of MTB magnetism. The magnetic guidance of these prokaryotes and eukaryotes is due to the biomineralization of magnetic crystals. This article provides a brief overview of the current knowledge concerning the different multicellular prokaryotes and micro/macroeukaryotes capable of magnetoreception. We also discuss the evolution of this unique ability.

ABSTRACT Magnetotactic bacteria (MTB) produce magnetosomes, which are sensory organelles consisting of nanocrystals of a magnetic iron mineral enclosed by membranes. In the well-characterized Magnetospirillum species of the Alphaproteobacteria, magnetosomes align and form highly ordered chains along filaments that consist of the bacterial actin homolog MamK. The MamK protein is part of a multi-component “magnetoskeleton” that controls the concatenation, positioning, and partitioning of the magnetosome chains (MCs) which serve as cellular compass for efficient navigation in the Earth’s magnetic field. MamK is highly conserved in all MTB; however, it is unknown whether its magnetoskeletal function is preserved, especially in those MTB which exhibit distinct and more complex architectures of MCs and often contain additional putative magnetoskeletal constituents such as the actin-like protein Mad28 with as yet-unknown functions. Here, we studied the ability of magnetosome-associated actins from a wide range of diverse MTB to rescue well-characterized magnetoskeleton mutants of the model Magnetospirillum gryphiswaldense. We found that MamK orthologs from Alpha-, Delta-, Candidatus Etaproteo-, and Nitrospirota-MTB as well as a resurrected MamK LUCA version restored MC assembly to varying degrees and exhibited filamentous localization in M. gryphiswaldense and E. coli. We also identified a novel magnetosome-related protein from the magnetotactic alphaproteobacterium Magnetovibrio blakemorei that substitutes the function of the well-characterized MamJ protein as a molecular adaptor tethering magnetosomes to MamK filaments. Moreover, we demonstrate that Mad28 orthologs from Thermodesulfobacteriota and Nitrospirota are actin-like proteins that can functionally complement mamK mutants of M. gryphiswaldense and which form filamentous structures in vivo and in vitro. IMPORTANCE To efficiently navigate within the geomagnetic field, magnetotactic bacteria (MTB) align their magnetosome organelles into chains, which are organized by the actin-like MamK protein. Although MamK is the most highly conserved magnetosome protein common to all MTB, its analysis has been confined to a small subgroup owing to the inaccessibility of most MTB. Our study takes advantage of a genetically tractable host where expression of diverse MamK orthologs together with a resurrected MamK LUCA and uncharacterized actin-like Mad28 proteins from deep-branching MTB resulted in gradual restoration of magnetosome chains in various mutants. Our results further indicate the existence of species-specific MamK interactors and shed light on the evolutionary relationships of one of the key proteins associated with bacterial magnetotaxis.