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Magnetic Guidance in Multicellular Prokaryotes and Eukaryotes
Abstract
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.
... Biomagnetism and biomagnets are everywhere. Whether precipitated by bacteria or by microorganisms in association with eukaryotes (see Leão and Lefèvre 2023 this issue), we are only just beginning to explore and understand the importance of biomagnetism to the natural world. While most studies point to the function of biomagnetism as navigation, questions remain regarding whether other functions exist, such as energy conservation. ...
Biomagnetism describes the biological origin of magnetism within living organisms. This phenomenon occurs due to the formation of iron-based minerals that exhibit magnetic ordering at room temperature. Perhaps the most studied form of biomagnetism originates in bacteria, especially magnetotactic bacteria that produce internal magnetite and greigite grains and iron-reducing bacteria that produce magnetite nanoparticles externally as a byproduct of iron respiration. These bacteria likely contribute to a significant proportion of environmental magnetite. The emergence of biomagnetism remains unclear, although it is thought that magnetotactic bacteria evolved this mechanism several billion years ago. Understanding how and why micro-organisms generate biomagnetism is helping to shed light on the origin of life on Earth and potentially on other planets. Biomagnetism is also of broad interest to industrial and environmental applications.
Microscopic and spectroscopic techniques are commonly applied to study microbial cells but are typically used on separate samples, resulting in population-level datasets that are integrated across different cells with little spatial resolution. To address this shortcoming, we developed a workflow that correlates several microscopic and spectroscopic techniques to generate an in-depth analysis of individual cells. By combining stable isotope probing (SIP), fluorescence in situ hybridization (FISH), scanning electron microscopy (SEM), confocal Raman microspectroscopy (Raman), and nano-scale secondary ion mass spectrometry (NanoSIMS), we illustrate how individual cells can be thoroughly interrogated to obtain information about their taxonomic identity, structure, physiology, and metabolic activity. Analysis of an artificial microbial community demonstrated that our correlative approach was able to resolve the activity of single cells using heavy water SIP in conjunction with Raman and/or NanoSIMS and establish their taxonomy and morphology using FISH and SEM. This workflow was then applied to a sample of yet uncultured multicellular magnetotactic bacteria (MMB). In addition to establishing their identity and activity, backscatter electron microscopy (BSE), NanoSIMS, and energy-dispersive X-ray spectroscopy (EDS) were employed to characterize the magnetosomes within the cells. By integrating these techniques, we demonstrate a cohesive approach to thoroughly study environmental microbes on a single-cell level.
Significance
We present a model of biogenic magnetite formation in eukaryotes and hypothesize this genetic mechanism is used by broad forms of life for geomagnetic sensory perception. Countering previous assertions that salmon olfactory tissues lack biogenic magnetite, we determine that it is present in the form of compact crystal clusters and show that a subset of genes differentially expressed in candidate magnetoreceptor cells, compared to nonmagnetic olfactory cells, are distant homologs to a core suite of genes utilized by magnetotactic bacteria for magnetite biomineralization. This same core gene suite is common to a broad array of eukaryotes and the Asgard clade archaea Lokiarchaeta. Findings have implications for revising our understanding of eukaryote magnetite biomineralization, sensory perception of magnetic fields, and eukaryogenesis.
Magnetotactic bacteria(MTB) are a group of prokaryotes having the ability to orient and swim along geomagnetic fi eld lines because they contain intracellular magnetosomes that are synthesized through a biomineralization process. Magnetosomes have recently also been found in unicellular eukaryotes, which are referred to as magnetically responsive protists(MRPs). The magnetosomes have three origins in MRPs. In this study, we characterized a MTB-grazing ciliated MRP that was magnetically collected from intertidal sediment of Huiquan Bay, Qingdao, China. Based on 18S rRNA gene sequence analysis, the ciliated MRP was tentatively identifi ed as Uronemella parafi lificum HQ. Using transmission electron microscopy, we observed that magnetosomes having 2-3 shapes were randomly distributed within this ciliate. Energydispersive X-ray spectroscopy and high-resolution transmission electron microscopy images of the magnetosomes were consistent with them being composed of magnetite. Magnetosomes having the same shape and mineral composition were also detected in MTB that occurred in the same environment as the ciliated MRP. Statistical analysis showed that the size and shape of the magnetosomes in the ciliated MRP were similar to those in MTB. The results suggest that this ciliated MRP can graze, ingest, and digest various types of MTB. It is certainly worth noting that this is the fi rst record of MRPs in Asian aquatic sediment and suggesting they might be widely distributed. These results also support the assertion that MRPs probably contribute to the ecological cycles of iron, and expand possibilities for research into the mechanism of magnetoreception in eukaryotes.
A broad range of organisms, from prokaryotes to higher animals, have the ability to sense and utilize Earth's geomagnetic field—a behavior known as magnetoreception. Although our knowledge of the physiological mechanisms of magnetoreception has increased substantially over recent decades, the origin of this behavior remains a fundamental question in evolutionary biology. Despite this, there is growing evidence that magnetic iron mineral biosynthesis by prokaryotes may represent the earliest form of biogenic magnetic sensors on Earth. Here, we integrate new data from microbiology, geology and nanotechnology, and propose that initial biomineralization of intracellular iron nanoparticles in early life evolved as a mechanism for mitigating the toxicity of reactive oxygen species (ROS), as ultraviolet radiation and free-iron-generated ROS would have been a major environmental challenge for life on early Earth. This iron-based system could have later been co-opted as a magnetic sensor for magnetoreception in microorganisms, suggesting an origin of microbial magnetoreception as the result of the evolutionary process of exaptation.
Here, the authors identify a mutualistic symbiosis between a non-motile, magnetic deltaproteobacterium and a protist, resulting in eukaryotic magnetoreception in marine anoxic sediments.
Magnetotactic bacteria (MTB) represent a group of microorganisms that are widespread in aquatic habitats and thrive at oxic-anoxic interfaces. They are able to scavenge high concentrations of iron thanks to the biomineralization of magnetic crystals in their unique organelles, the so-called magnetosome chains. Although their biodiversity has been intensively studied, their ecology and impact on iron cycling remain largely unexplored. Predation by protozoa was suggested as one of the ecological processes that could be involved in the release of iron back into the ecosystem. Magnetic protozoa were previously observed in aquatic environments, but their diversity and the fate of particulate iron during grazing are poorly documented. In this study, we report the morphological and molecular characterizations of a magnetically responsive MTB-grazing protozoan able to ingest high quantities of MTB. This protozoan is tentatively identified as Uronema marinum, a ciliate known to be a predator of bacteria. Using light and electron microscopy, we investigated in detail the vacuoles in which the lysis of phagocytized prokaryotes occurs. We carried out high-resolution observations of aligned magnetosome chains and ongoing dissolution of crystals. Particulate iron in the ciliate represented approximately 0.01% of its total volume. We show the ubiquity of this interaction in other types of environments and describe different grazing strategies. These data contribute to the mounting evidence that the interactions between MTB and protozoa might play a significant role in iron turnover in microaerophilic habitats.
SUMMARY Magnetotactic bacteria (MTB) are widespread, motile, diverse prokaryotes that biomineralize a unique organelle called the magnetosome. Magnetosomes consist of a nano-sized crystal of a magnetic iron mineral that is enveloped by a lipid bilayer membrane. In cells of almost all MTB, magnetosomes are organized as a well-ordered chain. The magnetosome chain causes the cell to behave like a motile, miniature compass needle where the cell aligns and swims parallel to magnetic field lines. MTB are found in almost all types of aquatic environments, where they can account for an important part of the bacterial biomass. The genes responsible for magnetosome biomineralization are organized as clusters in the genomes of MTB, in some as a magnetosome genomic island. The functions of a number of magnetosome genes and their associated proteins in magnetosome synthesis and construction of the magnetosome chain have now been elucidated. The origin of magnetotaxis appears to be monophyletic; that is, it developed in a common ancestor to all MTB, although horizontal gene transfer of magnetosome genes also appears to play a role in their distribution. The purpose of this review, based on recent progress in this field, is focused on the diversity and the ecology of the MTB and also the evolution and transfer of the molecular determinants involved in magnetosome formation.
Magnetosomes are prokaryotic organelles produced by magnetotactic bacteria that consist of nanometer-sized magnetite (Fe(3)O(4)) or/and greigite (Fe(3)S(4)) magnetic crystals enveloped by a lipid bilayer membrane. In magnetite-producing magnetotactic bacteria, proteins present in the magnetosome membrane modulate biomineralization of the magnetite crystal. In these microorganisms, genes that encode for magnetosome membrane proteins as well as genes involved in the construction of the magnetite magnetosome chain, the mam and mms genes, are organized within a genomic island. However, partially because there are presently no greigite-producing magnetotactic bacteria in pure culture, little is known regarding the greigite biomineralization process in these organisms including whether similar genes are involved in the process. Here using culture-independent techniques, we now show that mam genes involved in the production of magnetite magnetosomes are also present in greigite-producing magnetotactic bacteria. This finding suggest that the biomineralization of magnetite and greigite did not have evolve independently (that is, magnetotaxis is polyphyletic) as once suggested. Instead, results presented here are consistent with a model in which the ability to biomineralize magnetosomes and the possession of the mam genes was acquired by bacteria from a common ancestor, that is, the magnetotactic trait is monophyletic.
Some vertebrates can navigate over long distances using the Earth's magnetic field, but the sensory system that they use to do so has remained a mystery. Here we describe the key components of a magnetic sense underpinning this navigational ability in a single species, the rainbow trout (Oncorhynchus mykiss). We report behavioural and electrophysiological responses to magnetic fields and identify an area in the nose of the trout where candidate magnetoreceptor cells are located. We have tracked the sensory pathway from these newly identified candidate magnetoreceptor cells to the brain and associated the system with a learned response to magnetic fields.
Although ferrimagnetic material appears suitable as a basis of magnetic field perception in animals, it is not known by which mechanism magnetic particles may transduce the magnetic field into a nerve signal. Provided that magnetic particles have remanence or anisotropic magnetic susceptibility, an external magnetic field will exert a torque and may physically twist them. Several models of such biological magnetic-torque transducers on the basis of magnetite have been proposed in the literature. We analyse from first principles the conditions under which they are viable. Models based on biogenic single-domain magnetite prove both effective and efficient, irrespective of whether the magnetic structure is coupled to mechanosensitive ion channels or to an indirect transduction pathway that exploits the strayfield produced by the magnetic structure at different field orientations. On the other hand, torque-detector models that are based on magnetic multi-domain particles in the vestibular organs turn out to be ineffective. Also, we provide a generic classification scheme of torque transducers in terms of axial or polar output, within which we discuss the results from behavioural experiments conducted under altered field conditions or with pulsed fields. We find that the common assertion that a magnetoreceptor based on single-domain magnetite could not form the basis for an inclination compass does not always hold.
Magnetotactic algae of the genus Anisonema (Euglenophyceae) have been isolated from a coastal mangrove swamp in northeastern Brazil. The magnetotactic response is based on a permanent magnetic dipole moment per cell approximately 7 10(-10) emu. Each cell contains many magnetite (Fe(3)O(4)) particles organized in chains.
The magnetic compass of European robins does not use the polarity of the magnetic field for detecting the north direction. The birds derive their north direction from interpreting the inclination of the axial direction of the magnetic field lines in space, and they take the direction on the magnetic north-south axis for "north" where field lines and gravity vector form the smaller angle.
Magnetotactic bacteria show an ability to navigate along magnetic field lines because of magnetic particles called magnetosomes. All magnetotactic bacteria are unicellular except for the multicellular prokaryote (recently named 'Candidatus Magnetoglobus multicellularis'), which is formed by an orderly assemblage of 17-40 prokaryotic cells that swim as a unit. A ciliate was used in grazing experiments with the M. multicellularis to study the fate of the magnetosomes after ingestion by the protozoa. Ciliates ingested M. multicellularis, which were located in acid vacuoles as demonstrated by confocal laser scanning microscopy. Transmission electron microscopy and X-ray microanalysis of thin-sectioned ciliates showed the presence of M. multicellularis and magnetosomes inside vacuoles in different degrees of degradation. The magnetosomes are dissolved within the acidic vacuoles of the ciliate. Depending on the rate of M. multicellularis consumption by the ciliates the iron from the magnetosomes may be recycled to the environment in a more soluble form.
Biomagnetism describes the biological origin of magnetism within living organisms. This phenomenon occurs due to the formation of iron-based minerals that exhibit magnetic ordering at room temperature. Perhaps the most studied form of biomagnetism originates in bacteria, especially magnetotactic bacteria that produce internal magnetite and greigite grains and iron-reducing bacteria that produce magnetite nanoparticles externally as a byproduct of iron respiration. These bacteria likely contribute to a significant proportion of environmental magnetite. The emergence of biomagnetism remains unclear, although it is thought that magnetotactic bacteria evolved this mechanism several billion years ago. Understanding how and why micro-organisms generate biomagnetism is helping to shed light on the origin of life on Earth and potentially on other planets. Biomagnetism is also of broad interest to industrial and environmental applications.
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.
Under the same selection pressures, two genetically divergent populations may evolve in parallel toward the same adaptive solutions. Here, we hypothesized that magnetotaxis (i.e., magnetically guided chemotaxis) represents a key adaptation to micro-oxic habitats in aquatic sediments and that its parallel evolution homogenized the phenotypes of two evolutionary divergent clusters of freshwater spirilla. All magnetotactic bacteria affiliated to the Magnetospirillum genus (Alphaproteobacteria class) biomineralize the same magnetic particle chains and share highly similar physiological and ultrastructural features. We looked for the processes that could have contributed at shaping such an evolutionary pattern by reconciling species and gene trees using newly sequenced genomes of Magnetospirillum related bacteria. We showed that repeated horizontal gene transfers and homologous recombination of entire operons contributed to the parallel evolution of magnetotaxis. We propose that such processes could represent a more parsimonious and rapid solution for adaptation compared with independent and repeated de novo mutations, especially in the case of traits as complex as magnetotaxis involving tens of interacting proteins. Besides strengthening the idea about the importance of such a function in micro-oxic habitats, these results reinforce previous observations in experimental evolution suggesting that gene flow could alleviate clonal interference and speed up adaptation under some circumstances.
The most well recognized magnetoreception behavior is that of the magnetotactic bacteria (MTB), which synthesize membrane‐bounded magnetic nanocrystals called magnetosomes via a biologically controlled process. The magnetic minerals identified in prokaryotic magnetosomes are magnetite (Fe3O4) and greigite (Fe3S4). Magnetosome crystals, regardless of composition, have consistent, species‐specific morphologies and single‐domain size range. Because of these features, magnetosome magnetite crystals possess specific properties in comparison to abiotic, chemically‐synthesized magnetite. Despite numerous discoveries regarding MTB phylogeny over the last decades, this diversity is still considered underestimated. Characterization of magnetotactic microorganisms is important as it might provide insights into the origin and establishment of magnetoreception in general, including eukaryotes. Here we describe the magnetotactic behavior and characterize the magnetosomes from a flagellated protist using culture‐independent methods. Results strongly suggest that, unlike previously described magnetotactic protists, this flagellate is capable of biomineralizing its own anisotropic magnetite magnetosomes which are aligned in complex aggregations of multiple chains within the cell. This organism has a similar response to magnetic field inversions as MTB. Therefore, this eukaryotic species might represent an early origin of magnetoreception based on magnetite biomineralization. It should add to the definition of parameters and criteria to classify biogenic magnetite in the fossil record.
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Magnetotactic multicellular prokaryotes (MMPs) consist of unique microorganisms formed by genetically identical Gram-negative bacterial that live as a single individual capable of producing magnetic nano-particles called magnetosomes. Two distinct morphotypes of MMPs are known: spherical MMPs (sMMPs) and ellipsoidal MMPs (eMMPs). sMMPs have been extensively characterized, but less information exists for eMMPs. Here, we report the ultrastructure and organization as well as gene clusters responsible for magnetosome and flagella biosynthesis in the magnetite magnetosome producer eMMP Candidatus Magnetananas rongchenensis. Transmission electron microscopy and focused ion beam scanning electron microscopy (FIB-SEM) 3D reconstruction reveal that cells with a conspicuous core-periphery polarity were organized around a central space. Magnetosomes were organized in multiple chains aligned along the periphery of each cell. In the partially sequenced genome, magnetite-related mamAB gene and mad gene clusters were identified. Two cell morphologies were detected: irregular elliptical conical "frustum-like" (IECF) cells and H-shaped cells. IECF cells merge to form H-shaped cells indicating a more complex structure and possibly a distinct evolutionary position of eMMPs when compared to sMMPs considering multicellularity. This article is protected by copyright. All rights reserved.
Magnetotactic bacteria derive their magnetic orientation from magnetosomes, which are unique organelles that contain nanometre-sized crystals of magnetic iron minerals. Although these organelles have evident potential for exciting biotechnological applications, a lack of genetically tractable magnetotactic bacteria had hampered the development of such tools; however, in the past decade, genetic studies using two model Magnetospirillum species have revealed much about the mechanisms of magnetosome biogenesis. In this Review, we highlight these new insights and place the molecular mechanisms of magnetosome biogenesis in the context of the complex cell biology of Magnetospirillum spp. Furthermore, we discuss the diverse properties of magnetosome biogenesis in other species of magnetotactic bacteria and consider the value of genetically 'magnetizing' non-magnetotactic bacteria. Finally, we discuss future prospects for this highly interdisciplinary and rapidly advancing field. © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Significance
Billions of birds fly thousands of kilometers every year between their breeding and wintering grounds, helped by an extraordinary ability to detect the direction of the Earth’s magnetic field. The biophysical sensory mechanism at the heart of this compass is thought to rely on magnetically sensitive, light-dependent chemical reactions in cryptochrome proteins in the eye. Thus far, no theoretical model has been able to account for the <5° precision with which migratory birds are able to detect the geomagnetic field vector. Here, using computer simulations, we show that genuinely quantum mechanical, long-lived spin coherences in realistic models of cryptochrome can provide the necessary precision. The crucial structural and dynamical molecular properties are identified.
Optogenetic and chemogenetic actuators are critical for deconstructing the neural correlates of behavior. However, these tools have several limitations, including invasive modes of stimulation or slow on/off kinetics. We have overcome these disadvantages by synthesizing a single-component, magnetically sensitive actuator, "Magneto," comprising the cation channel TRPV4 fused to the paramagnetic protein ferritin. We validated noninvasive magnetic control over neuronal activity by demonstrating remote stimulation of cells using in vitro calcium imaging assays, electrophysiological recordings in brain slices, in vivo electrophysiological recordings in the brains of freely moving mice, and behavioral outputs in zebrafish and mice. As proof of concept, we used Magneto to delineate a causal role of striatal dopamine receptor 1 neurons in mediating reward behavior in mice. Together our results present Magneto as an actuator capable of remotely controlling circuits associated with complex animal behaviors.
For magnetic orientation, magnetotactic bacteria biosynthesize magnetosomes, which consist of membrane-enveloped magnetic nanocrystals of either magnetite (Fe3 O4 ) or greigite (Fe3 S4 ). While magnetite formation is increasingly well understood, much less is known about the genetic control of greigite biomineralization. Recently, two related yet distinct sets of magnetosome genes were discovered in a cultivated magnetotactic deltaproteobacterium capable of synthesizing either magnetite or greigite or both minerals. This led to the conclusion that greigite and magnetite magnetosomes are synthesized by separate biomineralization pathways. Although magnetosomes of both mineral types co-occured in uncultured multicellular magnetotactic prokaryotes (MMPs), so far only one type magnetosome genes could be identified in the available genome data. The MMP Candidatus Magnetomorum strain HK-1 from coastal tidal sand flats of the North Sea (Germany) was analyzed by a targeted single-cell approach. The draft genome assembly resulted in a size of 14.3 Mb and an estimated completeness of 95%. In addition to genomic features consistent with a sulfate-reducing lifestyle, we identified numerous genes putatively involved in magnetosome biosynthesis. Remarkably, most mam orthologs were present in two paralogous copies with highest similarity to either magnetite or greigite type magnetosome genes, supporting the ability to synthesize magnetite and greigite magnetosomes.
Bacteria containing magnetosomes (protein-bound nanoparticles of magnetite or greigite) are common to many sedimentary habitats, but have never been found before to live within another organism. Here, we show that octahedral inclusions in the extracellular symbionts of the marine bivalve Thyasira cf. gouldi contain iron, can exhibit magnetic contrast and are most likely magnetosomes. Based on 16S rRNA sequence analysis, T. cf. gouldi symbionts group with symbiotic and free-living sulfur-oxidizing, chemolithoautotrophic gammaproteobacteria, including the symbionts of other thyasirids. T. cf. gouldi symbionts occur both among the microvilli of gill epithelial cells and in sediments surrounding the bivalves, and are therefore facultative. We propose that free-living T. cf. gouldi symbionts use magnetotaxis as a means of locating the oxic-anoxic interface, an optimal microhabitat for chemolithoautotrophy. T. cf. gouldi could acquire their symbionts from near-burrow sediments (where oxic-anoxic interfaces likely develop due to the host's bioirrigating behavior) using their superextensile feet, which could transfer symbionts to gill surfaces upon retraction into the mantle cavity. Once associated with their host, however, symbionts need not maintain structures for magnetotaxis as the host makes oxygen and reduced sulfur available via bioirrigation and sulfur-mining behaviors. Indeed, we show that within the host, symbionts lose the integrity of their magnetosome chain (and possibly their flagellum). Symbionts are eventually endocytosed and digested in host epithelial cells, and magnetosomes accumulate in host cytoplasm. Both host and symbiont behaviors appear important to symbiosis establishment in thyasirids.The ISME Journal advance online publication, 10 June 2014; doi:10.1038/ismej.2014.93.
Magnetotactic bacteria produce iron oxides, iron sulfides or both in organelles called magnetosomes. Most of these bacteria are unicellular and biomineralize magnetite (Fe3O4). In contrast, multicellular magnetotactic prokaryotes (MMPs) consisting of several gram-negative cells have only been known to crystallize the magnetic iron sulfide greigite (Fe3S4). In this work, we describe MMPs that mineralize magnetite in bullet-shaped crystals. Another unusual aspect is that magnetite occurs either as the only crystals or together with greigite crystals. MMPs containing only greigite in the magnetosomes occur in the same environment. These findings show that morphology, ultrastructure, and behavior are the main characteristics of the MMPs, not the type of magnetic crystal biomineralized in the magnetosomes.
Horizontal gene transfer (HGT), the transfer of genetic material other than by descent, is thought to have played significant roles in the evolution and distribution of genes in prokaryotes. These include those responsible for the ability of motile, aquatic magnetotactic bacteria (MTB) to align and swim along magnetic field lines and the biomineralization of magnetosomes that are responsible for this behaviour. There is some genomic evidence that HGT might be responsible for the distribution of magnetosome genes in different phylogenetic groups of bacteria. For example, in the genomes of a number of MTB, magnetosome genes are present as clusters within a larger structure known as the magnetosome genomic island surrounded by mobile elements such as insertion sequences and transposases as well as tRNA genes. Despite this, there is no strong direct proof of HGT between these organisms. Here we show that a phylogenetic tree based on magnetosome protein amino acid sequences from a number of MTB was congruent with the tree based on the organisms' 16S rRNA gene sequences. This shows that evolution and divergence of these proteins and the 16S rRNA gene occurred similarly. This suggests that magnetotaxis originated monophyletically in the Proteobacteria phylum and implies that the common ancestor of all Proteobacteria was magnetotactic.
Berthold, P. 1999. Towards a comprehensive theory for the evolution, control and adaptability of avian migration. In: Adams, N.J. & Slotow, R.H. (eds) Roc. 22 Int. Ornithol. Congr., Durban. Ostrich 70 (1): 1–11.Theories about the evolution of migratory behaviour in birds have recently been grouped in eight categories (Rappole 1995). Common to all of them is the idea that migration originated in ancestral sedentary populations by some kind of ‘behavioural jump’. These are difficult to explain, especially under the assumption that migration has evolved several or many times independently. Recent experimental studies undertaken to illuminate the genetics of bird migration and the potential and speed of the associated microevolutionary processes have led to another view—a simple yet comprehensive theory. Its central concept is (obligate) partial migration, which is extremely widespread at higher latitudes, possibly also in the tropics, and seems to have evolved very early or might even have been inherited from pre-avian ancestors. Partial migration provides a behavioural turntable from which exclusive migratoriness and sedentariness can easily and rapidly be reached (or left) through selection and related microevolutionary processes. The fact that all important migratory features are directly genetically controlled, that migratoriness and amount of migratory activity are based on a common genetic mechanism, and that migratory syndromes exist, probably all greatly facilitate microevolutionary changes from migratoriness to sedentariness and vice versa.
Magnetite, the only known biogenic material with ferromagnetic properties, has been identified as a biochemical precipitate in three of the five kingdoms of living organisms, with a fossil record that now extends back nearly 2 billion years. In the magnetotactic bacteria, protoctists, and fish, single-domain crystals of magnetite are arranged in membrane-bound linear structures called magnetosomes, which function as biological bar magnets. Magnetosomes in all three of these groups bear an overall structural similarity to each other, which includes alignment of the individual crystallographic [111] directions parallel to the long axis. Although the magnetosomes represent only a small volume fraction in higher organisms, enough of these highly energetic structures are present to provide sensitivity to extremely small fluctuations and gradients in the background geomagnetic field. Previous experiments with elasmobranch fish are reexamined to test the hypothesis that gradients played a role in their successful geomagnetic conditioning, and a variety of four-turn coil designs are considered that could be used to test the various hypotheses proposed for them.
Chemical stratification occurs in the water columns and sediments of many aquatic habitats resulting in vertical chemical and redox gradients. Various types of microorganisms are often associated with specific depths and chemical parameters in these situations. For example, magnetite-producing magnetotactic bacteria are known to form horizontal "plates" of cells at the oxic/anoxic transition zone (OATZ) of such environments. Here, we report the presence of populations of diverse magnetic protists in a seasonally chemically stratified, coastal salt pond. The protistan types included several biflagellates, a dinoflagellate, and a ciliate that were each associated with specific depths and thus, specific chemical, microbiological and redox conditions in the water column. Most cells contained crystals of magnetite usually arranged in chains similar to the magnetosomes in the magnetotactic bacteria. The origin of the particles is unknown. There was no evidence of the presence of endosymbiotic magnetotactic bacteria within the protists nor were the protists observed to be engulfing magnetotactic bacteria despite the fact that high numbers of the latter were present at the same depths as the protists. However, this does not exclude ingestion of magnetotactic bacteria as a source of the magnetic particles while others may biomineralize magnetite. Because protists play an important role in the availability of iron for phytoplankton in marine waters by ingesting and reducing colloidal iron particles, the protists described here could play a significant role in iron cycling in chemically stratified anoxic basins, either through endogenous production of magnetic iron oxide and/or iron sulfide particles, or by ingestion of magnetotactic bacteria and the subsequent reduction and dissolution of iron oxide and/or sulfide particles in their magnetosomes.
Orientation, navigation, and homing are critical traits expressed by organisms ranging from bacteria through higher vertebrates. Sensory systems that aid such behavior have provided key selective advantages to these groups over the past 4 billion years, and are highly evolved; magnetoreception is no exception. Across many species and groups of organisms, compelling evidence exists that the physical basis of this response is tiny crystals of single-domain magnetite (Fe3O4). It is the opinion of the authors that all magnetic field sensitivity in living organisms, including elasmobranch fishes, is the result of a highly evolved, finely-tuned sensory system based on single-domain, ferromagnetic crystals.
With the use of different light and electron microscopic methods, we investigated the subcellular organization of afferent trigeminal terminals in the upper beak of the homing pigeon, Columba livia, which are about 5 microm in diameter and contain superparamagnetic magnetite (SPM) crystals. The SPM nanocrystals are assembled in clusters (diameter, approximately 1-2 microm). About 10 to 15 of these clusters occur inside one nerve terminal, arranged along the cell membrane. Each SPM cluster is embedded in a solid fibrous cup, open towards the cell surface, to which the cluster adheres by delicate fiber strands. In addition to the SPM clusters, a second inorganic iron compound has been identified: noncrystalline platelets of iron phosphate (about 500 nm wide and long and maximally 100 nm thick) that occur along a fibrous core of the terminal. The anatomic features suggested that these nerve endings could detect small intensity changes of the geomagnetic field. Such stimuli can induce deformations of the SPM clusters, which could be transduced into primary receptor potentials by mechanosensitive membrane receptor channels. The subepidermal fat cells surrounding the nerve endings prevent the inside from external mechanical stimuli. These structural findings corresponded to conclusions inferred from rock magnetic measurements, theoretical calculations, model experiments, and behavioral data, which also matched previous electrophysiologic recordings from migratory birds.