Multicellular Magnetotactic Prokaryotes Research Articles

Escape motility of multicellular magnetotactic prokaryotes.

Microorganisms often actively respond to multiple external stimuli to navigate toward their preferred niches. For example, unicellular magnetotactic bacteria integrate both oxygen sensory information and the Earth's geomagnetic field to help them locate anoxic conditions in a process known as magneto-aerotaxis. However, for multicellular magnetotactic prokaryotes (MMPs), the colonial structure of 4-16 cells places fundamental constraints on collective sensing, colony motility and directed swimming. To investigate how colonies navigate environments with multiple stimuli, we performed microfluidic experiments of MMPs with opposing magnetic fields and oxygen gradients. These experiments reveal unusual back-and-forth excursions called 'escape motility', in which colonies shuttle along magnetic field lines, punctuated by abrupt-yet highly coordinated-changes in collective ciliary beating. Through cell tracking and numerical simulations, we demonstrate that escape motility can arise through a simple magneto-aerotaxis mechanism, which includes the effect of magnetic torques and chemical sensing. At sufficiently high densities of MMPs, we observe the formation of dynamic crystal structures, whose stability is governed by the magnetic field strength and near-field hydrodynamic interactions. The results shed light on how some of the earliest multicellular organisms navigate complex physico-chemical landscapes.

Magnetic Guidance in Multicellular Prokaryotes and Eukaryotes

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.

Metagenomic and Microscopic Analysis of Magnetotactic Bacteria in Tangyin Hydrothermal Field of Okinawa Trough.

Magnetotactic bacteria (MTB) have been found in a wide variety of marine habitats, ranging from intertidal sediments to deep-sea seamounts. Deep-sea hydrothermal fields are rich in metal sulfides, which are suitable areas for the growth of MTB. However, MTB in hydrothermal fields have never been reported. Here, the presence of MTB in sediments from the Tangyin hydrothermal field was analyzed by 16S rRNA gene amplicon analysis, metagenomics, and transmission electron microscopy. Sequencing 16S rRNA gene yielded a total of 709 MTB sequences belonging to 20 OTUs, affiliated with Desulfobacterota, Alphaproteobacteria, and Nitrospirae. Three shapes of magnetofossil were identified by transmission electron microscopy: elongated-prismatic, bullet-shaped, and cuboctahedron. All of these structures were composed of Fe3O4. A total of 121 sequences were found to be homologous to the published MTB magnetosome-function-related genes, and relevant domains were identified. Further analysis revealed that diverse MTB are present in the Tangyin hydrothermal field, and that multicellular magnetotactic prokaryote (MMPs) might be the dominant MTB.

A Novel Isolate of Spherical Multicellular Magnetotactic Prokaryotes Has Two Magnetosome Gene Clusters and Synthesizes Both Magnetite and Greigite Crystals.

Multicellular magnetotactic prokaryotes (MMPs) are a unique group of magnetotactic bacteria that are composed of 10–100 individual cells and show coordinated swimming along magnetic field lines. MMPs produce nanometer-sized magnetite (Fe3O4) and/or greigite (Fe3S4) crystals—termed magnetosomes. Two types of magnetosome gene cluster (MGC) that regulate biomineralization of magnetite and greigite have been found. Here, we describe a dominant spherical MMP (sMMP) species collected from the intertidal sediments of Jinsha Bay, in the South China Sea. The sMMPs were 4.78 ± 0.67 μm in diameter, comprised 14–40 cells helical symmetrically, and contained bullet-shaped magnetite and irregularly shaped greigite magnetosomes. Two sets of MGCs, one putatively related to magnetite biomineralization and the other to greigite biomineralization, were identified in the genome of the sMMP, and two sets of paralogous proteins (Mam and Mad) that may function separately and independently in magnetosome biomineralization were found. Phylogenetic analysis indicated that the sMMPs were affiliated with Deltaproteobacteria. This is the first direct report of two types of magnetosomes and two sets of MGCs being detected in the same sMMP. The study provides new insights into the mechanism of biomineralization of magnetosomes in MMPs, and the evolutionary origin of MGCs.

Occurrence of south- and north-seeking multicellular magnetotactic prokaryotes in a coastal lagoon in the South Hemisphere.

Magnetotactic bacteria (MTB) response to the magnetic field can be classified into north-seeking (NS) and south-seeking (SS), which usually depends on their inhabiting site in the North and South Hemisphere, respectively. However, uncommon inverted polarity was observed on both hemispheres. Here, we studied magnetotactic multicellular prokaryotes (MMPs) from a coastal lagoon in Brazil collected in April and August 2014. MMPs from the first sampling period presented both magnetotactic behaviors, while MMPs collected in August/2014 were only SS. Phylogenetic analysis based on the 16S rRNA coding gene showed that these organisms belong to the Deltaproteobacteria class. The 16S rRNA gene sequences varied among MMPs regardless of the sampling period, and similarity values were not related to the type of magnetotactic response presented by the microorganisms. Therefore, differences in the magnetotactic behavior might result from the physiological state of MMPs, the availability of resources, or the instability of the chemical gradient in the environment. This is the first report of NS magnetotactic behavior on MMPs from the South Hemisphere.

Swimming behavior of the multicellular magnetotacticprokaryote 'Candidatus Magnetoglobus multicellularis' near solid boundaries and natural magnetic grains.

The magnetotactic yet uncultured species 'Candidatus Magnetoglobus multicellularis' is a spherical, multicellular ensemble of bacterial cells able to align along magnetic field lines while swimming propelled by flagella. Magnetotaxis is due to intracytoplasmic, membrane-bound magnetic crystals called magnetosomes. The net magnetic moment of magnetosomes interacts with local magnetic fields, imparting the whole microorganism a torque. Previous works investigated 'Ca. M. multicellularis' behavior when free swimming in water; however, they occur in sediments where bumping into solid particles must be routine. In this work, we investigate the swimming trajectories of 'Ca. M. multicellularis' close to solid boundaries using video microscopy. We applied magnetic fields 0.25-8.0mT parallel to the optical axis of a light microscope, such that microorganisms were driven upwards towards a coverslip. Because their swimming trajectories approach cylindrical helixes, circular profiles would be expected. Nevertheless, at fields 0.25-1.1mT, most trajectory projections were roughly sinusoidal, and net movements were approximately perpendicular to applied magnetic fields. Closed loops appeared in some trajectory projections at 1.1mT, which could indicate a transition to the loopy profiles observed at magnetic fields ≥ 2.15mT. The behavior of 'Ca. M. multicellularis' near natural magnetic grains showed that they were temporarily trapped by the particle's magnetic field but could reverse the direction of movement to flee away. Our results show that interactions of 'Ca. M. multicellularis with solid boundaries and magnetic grains are complex and possibly involve mechano-taxis.

Morphological and phylogenetic diversity of magnetotactic bacteria and multicellular magnetotactic prokaryotes from a mangrove ecosystem in the Sanya River, South China

Morphological and phylogenetic diversity of magnetotactic bacteria and multicellular magnetotactic prokaryotes from a mangrove ecosystem in the Sanya River, South China

Multicellularity makes the difference: multicellular magnetotactic prokaryotes have dynamic motion parameters dependent on the magnetic field intensity

Magnetotactic microorganisms can be found as unicellular entities, as coccus, vibrios, spirilla, rods and protists as well as multicellular organisms. The most studied multicellular magnetotactic prokaryote is “Candidatus Magnetoglobus multicellularis,” composed by an average number of 17 genetically identical magnetotactic bacteria. It is known that the magnetotactic orientation of “Ca. M. multicellularis” is different from the orientation shown by uncultured magnetotactic cocci. The present manuscript has the aim to compare the dynamic parameters of motion of both the magnetotactic microorganisms. U-turns trajectories were recorded, and one branch of the turn was used to get the trajectory parameters. The individual magnetic moment was estimated using the U-turn diameter. The parameters analyzed were the rotational drag coefficient, the kinetic energy, the flagellar force and the flagellar output power. From the rotational drag coefficient analysis, it was observed a difference among the experimental value and the expected value, and an “effective radius” is proposed to explain that difference. It was observed for the uncultured magnetotactic cocci that the kinetic energy, flagellar force and flagellar power are independent of the magnetic field intensity but for “Ca. M. multicellularis” an increase in these values was observed with the magnetic field intensification. It is proposed that the distribution of magnetic moments around the body of “Ca. M. multicellularis” is responsible for some magnetic force acting on its body in the presence of a uniform magnetic field. Also, the dynamic motion parameters calculated must support studies on the dynamic of motion of microorganisms.

Magnetoreception in multicellular magnetotactic prokaryotes: a new analysis of escape motility trajectories in different magnetic fields.

Magnetotactic microorganisms can be found as unicellular prokaryotes, as cocci, vibrions, spirilla and rods, and as multicellular organisms. Multicellular magnetotactic prokaryotes are magnetotactic microorganisms composed by several magnetotactic bacteria organized almost in a spherical helix, and one of the most studied is Candidatus Magnetoglobus multicellularis. Several studies have shown that Ca. M. multicellularis displays forms of behavior not well explained by magnetotaxis. One of these is escape motility, also known as "ping-pong" motion. Studies done in the past associated the "ping-pong" motion to some magnetoreceptive behavior, but those studies were never replicated. In the present manuscript a characterization of escape motility trajectories of Ca. M. multicellularis was done for several magnetic fields, considering that this microorganism swims in cylindrical helical trajectories. It was observed that the escape motility can be separated into three phases: (I) when the microorganism jumps from the drop border, (II) where the microorganism moves almost perpendicular to the magnetic field and (III) when the microorganism returns to the drop border. The total time of the whole escape motility, the time spent in phase II and the displacement distance in phase I decreases when the magnetic field increases. Our results show that the escape motility has several characteristics that depend on the magnetic field and cannot be understood by magnetotaxis, with a magnetoreceptive mechanism being the best explanation.

U-turn time and velocity dependence on the wavelength of light: multicellular magnetotactic prokaryotes of different sizes behave differently.

'Candidatus Magnetoglobus multicellularis' is a multicellular magnetotactic prokaryote found in the Araruama lagoon in Rio de Janeiro, Brazil. This microorganism shows a photokinesis that depends on the incident light wavelength, but that dependence can be canceled by the presence of radio-frequency (RF) electromagnetic fields. The present manuscript has as its aim to study the effect of light wavelength and RF fields on the U-turn time of 'Candidatus Magnetoglobus multicellularis', a behavior more related to magnetotaxis. As the experiments were performed during the night, the microorganisms were greater in size than normal, indicating that they were in the process of division. Our results show that when normal in size, the microorganism's U-turn time is modified by the light wavelength (lower for blue light than for green and red light), but RF fields do not affect that U-turn time dependence on the light wavelength. For the microorganism in the process of division, we describe for the first time how the photokinesis and U-turn time dependence on the light wavelength disappear. It is proposed that methyl-accepting chemotaxis proteins are involved in that light wavelength dependence for the U-turn time, but still more studies are necessary to understand how RF fields cancel the photokinesis light wavelength dependence, but do not affect the dependence of the U-turn time.

The swimming orientation of multicellular magnetotactic prokaryotes and uncultured magnetotactic cocci in magnetic fields similar to the geomagnetic field reveals differences in magnetotaxis between them.

Magnetotactic bacteria have intracellular chains of magnetic nanoparticles, conferring to their cellular body a magnetic moment that permits the alignment of their swimming trajectories to the geomagnetic field lines. That property is known as magnetotaxis and makes them suitable for the study of bacterial motion. The present paper studies the swimming trajectories of uncultured magnetotactic cocci and of the multicellular magnetotactic prokaryote 'Candidatus Magnetoglobus multicellularis' exposed to magnetic fields lower than 80μT. It was assumed that the trajectories are cylindrical helixes and the axial velocity, the helix radius, the frequency and the orientation of the trajectories relative to the applied magnetic field were determined from the experimental trajectories. The results show the paramagnetic model applies well to magnetotactic cocci but not to 'Ca. M. multicellularis' in the low magnetic field regime analyzed. Magnetotactic cocci orient their trajectories as predicted by classical magnetotaxis but in general 'Ca. M. multicellularis' does not swim following the magnetic field direction, meaning that for it the inversion in the magnetic field direction represents a stimulus but the selection of the swimming direction depends on other cues or even on other mechanisms for magnetic field detection.

Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes.

Multicellular magnetotactic prokaryotes (MMPs) exhibit peculiar coordination of swimming along geomagnetic field lines. Approximately 40-80 cells assemble, with a helical geometry or axisymmetry, into spherical or ellipsoidal MMPs respectively. To contribute to a comprehensive understanding of bacterial multicellularity here we took multiple microscopic approaches to study the diversity, assembly, reproduction and motility of ellipsoidal MMPs. Using correlative fluorescence in situ hybridization and scanning electron microscopy analysis, we found an unexpected diversity in populations of ellipsoidal MMPs in the Mediterranean Sea. The high-pressure freezing/freeze substitution fixation technique allowed us to show, for the first time, that cells adhere via juxtaposed membranes and are held together by a rimming lattice. Fluorescence confocal microscopy and ultrathin section images revealed not only the one-layer hollow three-dimensional architecture, but also periphery-core unilateral constriction of constituent cells and unidirectional binary fission of the ellipsoidal MMPs. This finding suggests the evolution toward MMPs multicellularity via the mechanism of incomplete separation of offspring. Remarkably, thousands of flagellar at the periphery surface of cells underpin the coordinated swimming of MMPs in response to mechanical, chemical, magnetic and optical stimuli, including a magnetotactic photokinesis behaviour. Together these results unveil the unique structure and function property of ellipsoidal MMPs.

Diversity and Characterization of Multicellular Magnetotactic Prokaryotes From Coral Reef Habitats of the Paracel Islands, South China Sea

While multicellular magnetotactic prokaryotes (MMPs) are ubiquitous in marine environments, the diversity of MMPs in sediments of coral reef ecosystems has rarely been reported. In this study, we made an investigation on the diversity and characteristics of MMPs in sediments at 11 stations in coral reef habitats of the Paracel Islands. The results showed that MMPs were present at nine stations, with spherical mulberry-like MMPs (s-MMPs) found at all stations and ellipsoidal pineapple-like MMPs (e-MMPs) found at seven stations. The maximum abundance of MMPs was 6 ind./cm3. Phylogenetic analysis revealed the presence of one e-MMP species and five s-MMP species including two species of a new genus. The results indicate that coral reef habitats of the Paracel Islands have a high diversity of MMPs that bio-mineralize multiple intracellular chains of iron crystals and play important role in iron cycling in such oligotrophic environment. These observations provide new perspective of the diversity of MMPs in general and expand knowledge of the occurrence of MMPs in coral reef habitats.

Association of magnetotactic multicellular prokaryotes with Pseudoalteromonas species in a natural lagoon environment.

Magnetotactic bacteria, for the most part, are free-living, motile, unicellular prokaryotes that inhabit almost all marine and freshwater environments. One notable exception to the unicellular mode, however, are the magnetotactic multicellular prokaryotes. These morphologically unique prokaryotes (e.g., Candidatus Magnetoglobus multicellularis) are motile aggregates of 20-40 genetically identical, Gram-negative cells organised as a sphere (or ovoid in shape) and only motile as a unit. No specific close physical association between magnetotactic bacteria and non-magnetotactic microorganisms has ever been reported. Here, using culture-independent approaches, we show an unusual association between the spherical magnetotactic multicellular prokaryote Ca. Magnetoglobus multicellularis and Pseudoalteromonas species in environmental sediment and water samples collected from the Araruama Lagoon in Brazil. Cells of Pseudoalteromonas species were observed to be physically attached to the surface and, notably, even in the intercellular space of these spherical magnetotactic multicellular prokaryotes. An attempt to correlate the frequency of association between Pseudoalteromonas and magnetotactic multicellular prokaryotes with sediment depth was made but only a slight decrease in the number of Pseudoalteromonas cells per magnetotactic multicellular prokaryote was observed with increasing depth. Similar observations were made with magnetotactic multicellular prokaryotes from another Brazilian Lagoon (Rodrigo de Freitas) and the putative symbiont/parasite was detected. Although our results suggest some sort of specificity in the relationship between these prokaryotes, the precise nature of this association remains unclear.

Seasonal changes in the vertical distribution of two types of multicellular magnetotactic prokaryotes in the sediment of Lake Yuehu, China.

There are two genetically distinct morphological types of multicellular magnetotactic prokaryotes (MMPs) in the intertidal zone of Lake Yuehu (China): ellipsoidal MMPs (eMMPs) and spherical MMPs (sMMPs). We studied the vertical distribution of both types of MMPs in the sediment at Lake Yuehu during 1 year. Both types of MMPs were observed at sediment depths ranging from 1 to 34 cm, depending on the seasons. The eMMPs distributed at depths of 2-34 cm during spring, 1-11 cm during summer, 2-21 cm during autumn and 9-32 cm during winter. The eMMP species Candidatus Magnetananas rongchenensis, with magnetite magnetosomes, dominated at all distribution depths. These results suggested that Ca. M. rongchenensis migrated vertically during four seasons. The vertical profiles of oxidation-reduction potential (ORP) in Lake Yuehu changed seasonally, and these changes coincided with the seasonal distribution of MMPs, suggesting that the ORP affected the vertical distribution of MMPs. In addition, high concentrations of ammonium and silicate were associated with low abundances of MMPs.

Effect of applied magnetic fields on motility and magnetotaxis in the uncultured magnetotactic multicellular prokaryote 'Candidatus Magnetoglobus multicellularis'.

Magnetotactic bacteria are found in the chemocline of aquatic environments worldwide. They produce nanoparticles of magnetic minerals arranged in chains in the cytoplasm, which enable these microorganisms to align to magnetic fields while swimming propelled by flagella. Magnetotactic bacteria are diverse phylogenetically and morphologically, including cocci, rods, vibria, spirilla and also multicellular forms, known as magnetotactic multicellular prokaryotes (MMPs). We used video-microscopy to study the motility of the uncultured MMP 'Candidatus Magnetoglobus multicellularis' under applied magnetic fields ranging from 0.9 to 32 Oersted (Oe). The bidimensional projections of the tridimensional trajectories where interpreted as plane projections of cylindrical helices and fitted as sinusoidal curves. The results showed that 'Ca. M. multicellularis' do not orient efficiently to low magnetic fields, reaching an efficiency of about 0.65 at 0.9-1.5 Oe, which are four to six times the local magnetic field. Good efficiency (0.95) is accomplished for magnetic fields ≥10 Oe. For comparison, unicellular magnetotactic microorganisms reach such efficiency at the local magnetic field. Considering that the magnetic moment of 'Ca. M. multicellularis' is sufficient for efficient alignment at the Earth's magnetic field, we suggest that misalignments are due to flagella movements, which could be driven by photo-, chemo- and/or other types of taxis.

X-ray Absorption Spectroscopy and Magnetism of Synthetic Greigite and Greigite Magnetosomes in Magnetotactic Bacteria

ABSTRACTScanning transmission X-ray microscopy at the Fe 2p (L2,3), O1s, C1s, and S2p edges was used to study greigite magnetosomes and other cellular content of a magnetotactic bacterium known as a multicellular magnetotactic prokaryote (MMP). X-ray absorption spectrum (XAS) and X-ray magnetic circular dichroism (XMCD) spectra of greigite (Fe3S4) nanoparticles, synthesized via a hydrothermal method, were measured. Although XAS of the synthetic greigite nanoparticles and biotic magnetosome crystals in MMPs are slightly different due to partial oxidation of the MMP greigite, the XMCD spectra of the two materials are in good agreement. The Fe 2p XAS and XMCD spectra of Fe3S4 are quite different from those of its oxygen analog, magnetite (Fe3O4), suggesting Fe3S4 has a different electronic and magnetic structure than Fe3O4 despite having the same crystal structure. Sulfate and sulfide species were also identified in MMPs, both of which are likely involved in sulfur metabolism.

Ultrastructure of ellipsoidal magnetotactic multicellular prokaryotes depicts their complex assemblage and cellular polarity in the context of magnetotaxis.

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 with sMMPs considering multicellularity.

The swimming polarity of multicellular magnetotactic prokaryotes can change during an isolation process employing magnets: evidence of a relation between swimming polarity and magnetic moment intensity.

Magnetotactic microorganisms are characterized by swimming in the direction of an applied magnetic field. In nature, two types of swimming polarity have been observed: north-seeking microorganisms that swim in the same direction as the magnetic field, and south-seeking microorganisms that swim in the opposite direction. The present work studies the reversal in the swimming polarity of the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis following an isolation process using high magnetic fields from magnets. The proportion of north- and south-seeking organisms was counted as a function of the magnetic field intensity used during the isolation of the organisms from sediment. It was observed that the proportion of north-seeking organisms increased when the magnetic field was increased. The magnetic moment for north- and south-seeking populations was estimated using the U-turn method. The average magnetic moment was higher for north- than south-seeking organisms. The results suggest that the reversal of swimming polarity must occur during the isolation process in the presence of high magnetic fields and magnetic field gradients. It is shown for the first time that the swimming polarity reversal depends on the magnetic moment intensity of multicellular magnetotactic prokaryotes, and new studies must be undertaken to understand the role of magnetic moment polarity and oxygen gradients in determination of swimming polarity.

Light effects on the multicellular magnetotactic prokaryote 'Candidatus Magnetoglobus multicellularis' are cancelled by radiofrequency fields: the involvement of radical pair mechanisms.

'Candidatus Magnetoglobus multicellularis' is the most studied multicellular magnetotactic prokaryote. It presents a light-dependent photokinesis: green light decreases the translation velocity whereas red light increases it, in comparison to blue and white light. The present article shows that radio-frequency electromagnetic fields cancel the light effect on photokinesis. The frequency to cancel the light effect corresponds to the Zeeman resonance frequency (DC magnetic field of 4Oe and radio-frequency of 11.5MHz), indicating the involvement of a radical pair mechanism. An analysis of the orientation angle relative to the magnetic field direction shows that radio-frequency electromagnetic fields disturb the swimming orientation when the microorganisms are illuminated with red light. The analysis also shows that at low magnetic fields (1.6Oe) the swimming orientation angles are well scattered around the magnetic field direction, showing that magnetotaxis is not efficiently in the swimming orientation to the geomagnetic field. The results do not support cryptochrome as being the responsible chromophore for the radical pair mechanism and perhaps two different chromophores are necessary to explain the radio-frequency effects.