**2.1 Cell biology**

MTB comprise a diverse group of prokaryotes that share the ability to synthesize magnetosomes, which are composed by a magnetic nanocrystal, magnetite (Fe3O4), or greigite (Fe3S4), enclosed by a lipid bilayer (**Figure 1**; [2]). Thus, MTB has no taxonomic meaning regarding phylogeny, morphology, and physiology. The morphology of cultured and uncultured MTB described until now are cocci, spirilla, rods, ovoids, vibrios, and multicellular spherical/ellipsoidal forms [5]. In all morphotypes, magnetosomes are arranged in one or multiple chains along the major axis of the cell, imparting the cell a magnetic moment, as mentioned previously [2]. However, in some uncultured MTB, apparently disorganized chains have already been observed [6, 7]. Besides the magnetosomes, other common features are the Gram-negative cell wall structure, motility by flagella and lipid, polyphosphate and sulfur inclusions [2].

MTB present microaerophilic or anaerobic metabolism and all inhabit aquatic environments characterized by vertical chemical stratification [2]. When observing a drop of environmental sample containing MTB on a light microscope with a magnet next to the slide, MTB tend to accumulate in one of the borders of the drop, which correspond to a magnetic pole, North or South. In the Southern Hemisphere, when MTB are being observed they usually accumulate at the border of the drop of sample corresponding to the magnet's North magnetic pole, swimming to Geomagnetic South pole indicated by a compass. Therefore, these bacteria are

#### **Figure 1.**

*Transmission electron microscopy of the magnetotactic bacterium* Magnetovibrio blakemorei *strain MV-1 showing a single chain of prismatic magnetite magnetosomes.*

#### *Biology and Physics of Magnetotactic Bacteria DOI: http://dx.doi.org/10.5772/intechopen.79965*

independently by Salvatore Bellini in 1963 and Richard Blakemore in 1975 [3]. The first to observe MTB was Salvatore Bellini, an Italian physician from Pavia, Italy. In 1958, physicians from Pavia were asked to analyze the quality of water for human consume. Bellini was part of the team that studied the water quality, and he observed in water samples some bacteria that consistently accumulate in one side of water drops. After trying different stimuli, he discovered that they were affected by magnets. He called that bacteria as magnetosensitive. The first published observation of MTB was done in 1975 by Richard Blakemore in Massachusetts, USA [4]. His discovery was accidental, because his goal was to isolate *Spirochaeta plicatilis* from marine marsh muds. During his observations, he noted microorganisms migrating to one end of the drop of the mud on the microscope slide, and discover

that the presence of magnets altered their swimming direction. He called

MTB comprise a diverse group of prokaryotes that share the ability to synthesize magnetosomes, which are composed by a magnetic nanocrystal, magnetite (Fe3O4), or greigite (Fe3S4), enclosed by a lipid bilayer (**Figure 1**; [2]). Thus, MTB has no taxonomic meaning regarding phylogeny, morphology, and physiology. The morphology of cultured and uncultured MTB described until now are cocci, spirilla, rods, ovoids, vibrios, and multicellular spherical/ellipsoidal forms [5]. In all

morphotypes, magnetosomes are arranged in one or multiple chains along the major axis of the cell, imparting the cell a magnetic moment, as mentioned previously [2]. However, in some uncultured MTB, apparently disorganized chains have already been observed [6, 7]. Besides the magnetosomes, other common features are the Gram-negative cell wall structure, motility by flagella and lipid, polyphosphate and

MTB present microaerophilic or anaerobic metabolism and all inhabit aquatic environments characterized by vertical chemical stratification [2]. When observing a drop of environmental sample containing MTB on a light microscope with a magnet next to the slide, MTB tend to accumulate in one of the borders of the drop, which correspond to a magnetic pole, North or South. In the Southern Hemisphere, when MTB are being observed they usually accumulate at the border of the drop of sample corresponding to the magnet's North magnetic pole, swimming to Geomagnetic South pole indicated by a compass. Therefore, these bacteria are

*Transmission electron microscopy of the magnetotactic bacterium* Magnetovibrio blakemorei *strain MV-1*

*showing a single chain of prismatic magnetite magnetosomes.*

magnetotaxis as the tactic response to magnetic fields.

**2. Biology of magnetotactic bacteria**

**2.1 Cell biology**

*Microorganisms*

sulfur inclusions [2].

**Figure 1.**

**4**

called South-seeking. In the Northern Hemisphere, the opposite situation occurs and MTB presenting this behavior are called North-seeking.

The study of MTB movement in an oxygen gradient showed that MTB change flagellar rotation and, consequently, the direction of movement depending on the oxygen concentration, migrating to the optimal conditions [8]. These observations were used to infer MTB dislocation along the vertical chemical gradient in the environment, which is based on the vertical component of the magnetic field and depends on the cellular state regarding oxygen. In the upper layers of the chemically stratified environment, where oxygen is abundant and higher than the optimal for MTB growth, the bacterium is on the oxidized state and rotate flagella to migrate downward, where the environment is more reduced. While in reducing conditions, in which oxygen is not abundant and concentrations are lower than that required for MTB growth, bacteria rotate the flagella in the opposite direction to reach upper layers of the gradient with optimal oxygen concentrations. Therefore, the presence of specific cell structures in MTB, as the magnetosome chain, flagella, and storage inclusions, represent adaptive advantages for dislocation across the chemical gradient to explore resources in the environment. For example, during the day, the oxygen gradient changes among the stratified layers of the environment and microorganisms dislocate across these layers to reach regions with suitable conditions for survival and growth. Because MTB are microaerophilic and/or capable of anaerobic respiration, which means that they are sensitive to high oxygen concentrations, an efficient mechanism to orient and migrate in the environment guarantees species survival.

Only a few species of MTB have been isolated in axenic cultures [9], and fewer type strains are available in cell line repositories. Many uncultured MTB species have been characterized from environmental samples, because it is possible to purify these cells based on their response to an applied magnetic field using a magnet [10]. **Figure 2** shows examples of cultured and uncultured species of MTB and their characteristics according to their phylogenetic affiliation. Note that MTB are spread among different phyla in Bacteria domain and that greigite magnetosomes are only synthesized by MTB belonging to Deltaproteobacteria class.

*Magnetospirillum* species, which include *M. gryphiswaldense* strain MSR-1, *M. magneticum* strain AMB-1, and *M. magnetotacticum* strain MS-1, among other strains, are spirilla with flagella at each pole of the cell and represent the most characterized MTB. Information about the biomineralization process and magnetosome organization within the cell is mainly based on species belonging to this genus [11]. Cryoelectron tomography studies using *M. magneticum* strain AMB-1 have shown that the magnetosome vesicle is a result of the cytoplasmic membrane invagination, which occurs before the synthesis of the magnetite nanocrystal [11, 12]; forming the magnetosome membrane vesicle in which proteins related to the biomineralization will be anchored. These proteins that are involved in all steps of the magnetosome formation are anchored to this invaginated portion of the membrane and will participate in the process by recruiting other proteins that integrate the process, for example, iron transport, crystal nucleation and growth, size and shape control, and organization of the magnetosomes [11, 13].

According to studies performed in *M. gryphiswaldense* strain MSR-1, mature magnetite magnetosomes are found already organized in a chain within the cytoplasm of the cell 15 min after formation has started [14]. All *Magnetospirillum* species produce a single chain of cuboctahedral magnetite magnetosomes that are 40–45 nm in size [10]. Other MTB species are capable of synthesizing magnetite magnetosomes with cuboctahedral, prismatic, or anisotropic shapes [2] and/or greigite magnetosomes, which are usually classified as irregular. Usually, a magnetotactic bacterium species is capable of producing magnetosomes with one

individual flagella and promote efficient swimming at high speed [20]. One of the

magnetotactic multicellular prokaryotes (MMP), which can be divided into spherical and ellipsoidal. MMP are formed by Gram-negative magnetotactic cells organized in a sphere that swims as a unit [21]. Cellular organization in MMP is not random and represents the best configuration to optimize the magnetic response of the microorganism [22]. These microorganisms present an exclusive multicellular life cycle in which cells of the microorganisms grow, divide, and rearrange before splitting into two identical multicellular microorganisms [23]. Individual cells of this type of MTB have never been observed and viability assays suggest that when a cell disaggregates from the multicellular structures, it does not remain viable [24]. MMPs are capable of synthesizing irregular greigite or bullet-shaped magnetosomes [21]. MMPs with both types of magnetosomes have already been reported [25].

The origin of magnetotaxis and its distribution among the different phyla of the Bacteria domain are not well understood. Despite the great phylogenetic diversity, MTB have unique genes related to biomineralization, which are located in a generally unstable region in the genome [26]. The genomic and ultrastructure characterizations of nonmagnetotactic spontaneous mutants of *M. gryphiswaldense* strain MSR-1 showed the absence of 130 kb genomic region and complete lack of

magnetosomes within these cells [27]. Genomic comparison among MTB affiliated to different phyla showed that genes in this region are conserved within MTB group, even when magnetite- and greigite-producing MTB were analyzed [11]. This region containing the genes responsible for the synthesis of magnetosomes was named magnetosome island and the genes are referred to as *mam* (*magnetosome membrane*), *mms* (*magnetosome membrane specific*), and *mtx* (*m*agne*t*ota*x*is) genes because proteins encoded by these genes are localized on the magnetosome mem-

The genes for biomineralization are grouped into four operons in *M. gryphiswaldense* strain MSR-1 and other freshwater spirilla, called *mamAB*,

In the past years, hypotheses were elaborated to explain the evolution of magnetotaxis. One of them was based on the observation that the evolution and divergence of the conserved Mam proteins and the 16S rRNA gene among MTB are congruent and support the monophyletic origin, in which all MTB would present a single common ancestor [9]. The other hypothesis states that the present diversity of MTB and magnetotaxis-related gene distribution is a result of multiple events of horizontal gene transfer, possibly with a common ancestral, gene modification and/ or loss in different cell lines [26]. Functional analysis of the magnetosome island based on deletion of genes in *Ms. gryphiswaldense* strain MSR-1 indicated that genes

*mamGFDC*, *mms6,* and *mamXY* in the magnetosome island [28]. Although species of MTB have different sizes in the region that encompasses the genes involved in biomineralization, some genes are conserved in all species. The content and organization of genes on the magnetosome island vary between magnetotactic species, and often, some genes are deleted or inserted without any change in the formation of the magnetosomes [27]. In general, proteins encoded by *mam* genes are involved in four major steps of magnetosome formation. These steps include: (1) formation of the magnetosome membrane (MamI, MamL, and MamAB); (2) formation of magnetite crystal (MamE, Mms6, MamB, and MamM); (3) maturation of the magnetite crystal (MamE, MmsF, MamGFDC, and Mam P, S, T); and (4) alignment of the chain magnetosome (MamJ and MamK) [29]. The mechanism by which these genes were and can be transferred between species of bacteria is unknown till date.

brane or participate on the magnetotaxis motility behavior.

most peculiar morphotype of MTB are the multicellular forms, named

*Biology and Physics of Magnetotactic Bacteria DOI: http://dx.doi.org/10.5772/intechopen.79965*

**2.2 Genetics**

**7**

#### **Figure 2.**

*Phylogenetic tree based on the 16S rRNA gene showing the distribution of some cultured and uncultured MTB in Nitrospirae and Proteobacteria phylum of Bacteria domain. White lines separate morphotypes of MTB in Proteobacteria phylum, showing the distribution of spirilla, vibrios, cocci, including ovoid and* fava*-like cells, rods, and multicellular microorganisms. The shape of magnetosomes found in each morphotypes also displayed next to the cells. However, it is important to remember that each MTB species is usually capable of producing only one type of magnetosome (composition and shape). Morphotypes labeled with an asterisk (\*) are the only capable of producing greigite magnetosomes; some of them, for example,* Desulfamplus magnetovallimortis *strain BW-1 produces both types of magnetosomes, irregular greigite and bullet-shaped magnetite magnetosomes.*

mineral composition and regular size and shape [15]. Rarely, a magnetotactic bacterium is capable of producing both magnetite and greigite magnetosomes; when it occurs, these magnetosomes with different composition and shape are arranged in the same chain(s) [16, 17]. Although differences have been observed in the formation of magnetosomes in MTB species [12, 18], the process described for bacteria belonging to *Magnetospirillum* genus is considered the model of magnetite biomineralization in MTB.

In the environment, magnetotactic cocci are the most abundant morphotype of MTB and present high phylogenetic diversity and variety of size, shape, and organization of magnetosomes [10, 19]. For example, magnetotactic cocci have been found in marine sediments from Antarctica, suggesting the existence of psychrophilic MTB [7]. Interestingly, these samples presented at least three types of magnetotactic cocci based on the magnetosomes crystal size, shape, and organization [7]. Ultrastructure characterization of cultured magnetotactic cocci showed that these cells present two bundles of flagella and can achieve speed of approximately 300 μm/s, which is extremely high if we consider that the bacterium has nearly 1 μm. Each flagellar apparatus of *Magnetococcus massalia* strain MO-1 is formed by seven flagellar filaments surrounded by a sheath that might interact with the bundle of flagella to decrease the friction of the high-speed rotation of

*Biology and Physics of Magnetotactic Bacteria DOI: http://dx.doi.org/10.5772/intechopen.79965*

individual flagella and promote efficient swimming at high speed [20]. One of the most peculiar morphotype of MTB are the multicellular forms, named magnetotactic multicellular prokaryotes (MMP), which can be divided into spherical and ellipsoidal. MMP are formed by Gram-negative magnetotactic cells organized in a sphere that swims as a unit [21]. Cellular organization in MMP is not random and represents the best configuration to optimize the magnetic response of the microorganism [22]. These microorganisms present an exclusive multicellular life cycle in which cells of the microorganisms grow, divide, and rearrange before splitting into two identical multicellular microorganisms [23]. Individual cells of this type of MTB have never been observed and viability assays suggest that when a cell disaggregates from the multicellular structures, it does not remain viable [24]. MMPs are capable of synthesizing irregular greigite or bullet-shaped magnetosomes [21]. MMPs with both types of magnetosomes have already been reported [25].

#### **2.2 Genetics**

The origin of magnetotaxis and its distribution among the different phyla of the Bacteria domain are not well understood. Despite the great phylogenetic diversity, MTB have unique genes related to biomineralization, which are located in a generally unstable region in the genome [26]. The genomic and ultrastructure characterizations of nonmagnetotactic spontaneous mutants of *M. gryphiswaldense* strain MSR-1 showed the absence of 130 kb genomic region and complete lack of magnetosomes within these cells [27]. Genomic comparison among MTB affiliated to different phyla showed that genes in this region are conserved within MTB group, even when magnetite- and greigite-producing MTB were analyzed [11]. This region containing the genes responsible for the synthesis of magnetosomes was named magnetosome island and the genes are referred to as *mam* (*magnetosome membrane*), *mms* (*magnetosome membrane specific*), and *mtx* (*m*agne*t*ota*x*is) genes because proteins encoded by these genes are localized on the magnetosome membrane or participate on the magnetotaxis motility behavior.

The genes for biomineralization are grouped into four operons in *M. gryphiswaldense* strain MSR-1 and other freshwater spirilla, called *mamAB*, *mamGFDC*, *mms6,* and *mamXY* in the magnetosome island [28]. Although species of MTB have different sizes in the region that encompasses the genes involved in biomineralization, some genes are conserved in all species. The content and organization of genes on the magnetosome island vary between magnetotactic species, and often, some genes are deleted or inserted without any change in the formation of the magnetosomes [27]. In general, proteins encoded by *mam* genes are involved in four major steps of magnetosome formation. These steps include: (1) formation of the magnetosome membrane (MamI, MamL, and MamAB); (2) formation of magnetite crystal (MamE, Mms6, MamB, and MamM); (3) maturation of the magnetite crystal (MamE, MmsF, MamGFDC, and Mam P, S, T); and (4) alignment of the chain magnetosome (MamJ and MamK) [29]. The mechanism by which these genes were and can be transferred between species of bacteria is unknown till date. In the past years, hypotheses were elaborated to explain the evolution of magnetotaxis. One of them was based on the observation that the evolution and divergence of the conserved Mam proteins and the 16S rRNA gene among MTB are congruent and support the monophyletic origin, in which all MTB would present a single common ancestor [9]. The other hypothesis states that the present diversity of MTB and magnetotaxis-related gene distribution is a result of multiple events of horizontal gene transfer, possibly with a common ancestral, gene modification and/ or loss in different cell lines [26]. Functional analysis of the magnetosome island based on deletion of genes in *Ms. gryphiswaldense* strain MSR-1 indicated that genes

**7**

mineral composition and regular size and shape [15]. Rarely, a magnetotactic bacterium is capable of producing both magnetite and greigite magnetosomes; when it occurs, these magnetosomes with different composition and shape are arranged in the same chain(s) [16, 17]. Although differences have been observed in the formation of magnetosomes in MTB species [12, 18], the process described for bacteria belonging to *Magnetospirillum* genus is considered the model of magnetite biomin-

*strain BW-1 produces both types of magnetosomes, irregular greigite and bullet-shaped magnetite*

*Phylogenetic tree based on the 16S rRNA gene showing the distribution of some cultured and uncultured MTB in Nitrospirae and Proteobacteria phylum of Bacteria domain. White lines separate morphotypes of MTB in Proteobacteria phylum, showing the distribution of spirilla, vibrios, cocci, including ovoid and* fava*-like cells, rods, and multicellular microorganisms. The shape of magnetosomes found in each morphotypes also displayed next to the cells. However, it is important to remember that each MTB species is usually capable of producing only one type of magnetosome (composition and shape). Morphotypes labeled with an asterisk (\*) are the only capable of producing greigite magnetosomes; some of them, for example,* Desulfamplus magnetovallimortis

In the environment, magnetotactic cocci are the most abundant morphotype of MTB and present high phylogenetic diversity and variety of size, shape, and organization of magnetosomes [10, 19]. For example, magnetotactic cocci have been found in marine sediments from Antarctica, suggesting the existence of psychrophilic MTB [7]. Interestingly, these samples presented at least three types of magnetotactic cocci based on the magnetosomes crystal size, shape, and organization [7]. Ultrastructure characterization of cultured magnetotactic cocci showed that these cells present two bundles of flagella and can achieve speed of approximately 300 μm/s, which is extremely high if we consider that the bacterium has nearly 1 μm. Each flagellar apparatus of *Magnetococcus massalia* strain MO-1 is formed by seven flagellar filaments surrounded by a sheath that might interact with

the bundle of flagella to decrease the friction of the high-speed rotation of

eralization in MTB.

**6**

**Figure 2.**

*Microorganisms*

*magnetosomes.*

in the *mamAB* operon are sufficient for magnetosome biomineralization [30]. Examples of genes found in this operon and their functions are listed in **Table 1**. Interestingly, the transference of genes from the *mamAB* operon from *M. gryphiswaldense* strain MSR-1 to *Rhodospirillum rubrum* resulted in magnetite magnetosome production within the photosynthetic cell [39]. Because of the magnetic properties of magnetosomes, which will be discussed on the following topic, these nanometric magnetic structures have great importance for the development of new applications and processes in Biotechnology. However, one of the limitations of their use in biotechnological applications is the fastidiousness of MTB, which makes the production of magnetosomes in bioreactors expensive and with low yield. The transference of the ability to synthesize magnetosomes from MTB to

other cells represents a new frontier in Microbiology and greatly expands the use of

Two different processes of mineral formation by living beings have been recognized. One process of mineral formation is known as biologically induced mineralization (BIM), and is characterized by bulk extracellular and/or intercellular mineral formation, without the elaboration of organic matrices. It produces minerals having crystal habits similar to those produced by precipitation from inorganic solutions. BIM processes are less controlled than organic matrix-mediated mineralization, and looks like a primitive stage in the evolution of biogenic mineral formation. The other process is known as biologically controlled mineralization (BCM). In general, the organism constructs an organic mold into which the appropriate ions are actively introduced to crystallize a mineral. The mineral type, orientation of crystallographic axes, and microarchitectures are under genetic control [40]. Magnetotactic bacteria distinguish from other bacteria because they biomineralize, through BCM, magnetic nanoparticles of magnetite, or greigite. Magnetite is a very interesting iron oxide because it is magnetic and a good conductor. Its free charge density is similar to that of some metals [41]. It is also a hard mineral, being used by chitons for tooth hardening [42]. Several studies show that greigite has similar electrical [43] and hardening use [44] as magnetite. The magnetic properties of nanoparticles have a strong dependence on the size: very small particles have a magnetic moment nonstable in the body, changing randomly its orientation and producing a null average magnetic moment. Those particles are known as superparamagnetic. If the size increases, the anisotropic energy also increases and creates an energy barrier that maintains the magnetic moment in a fixed direction. In that case, the nanoparticles behave as stable magnets and are known as single domains [45]. Magnetosomes are in the size range of magnetic single domains. The magnetic flux lines created by the magnetosome in the chain can be observed using the magnetic electron holography technique [46], showing the flux lines entirely aligned to the chain as corresponds with a dipolar field created by a single magnetic moment. So, it is appropriate to say that the magnetosome chain behaves as a compass needle. The linear arrange of magnetosomes is not energetically stable, because after some number of magnetosomes the best configuration is a ring. To maintain the linear configuration, magnetosomes are attached

The first analysis done in magnetosomes was energy-dispersive X-ray microanalysis (EDS or EDX), showing that they are composed mainly by iron and oxygen [4]. To show that they are the iron oxide magnetite, the Mossbauer technique was used [48], showing that the Mossbauer spectra behave as a mixture of magnetite

corresponding to magnetite [49]. Several studies with EDS show that this magnetite is highly pure. However, in some cases, some metallic ions can be absorbed in the magnetosome structure, depending on the ambient pollution [50]. Studies done with high-resolution electron microscopy show that magnetosomes are produced in

and maghemite. Also, electron diffraction shows the diffraction patterns

specific geometric morphologies [51]. Those morphologies are truncated cuboctahedron, elongated cuboctahedron, and hexagonal prisms. In the case of greigite, the crystalline morphologies are truncated cuboctahedrons and elongated rectangular prisms [51]. This iron sulfide was discovered in magnetosomes of multicellular magnetotactic prokaryotes, and identified through EDX spectroscopy

magnetosomes in nanotechnological and biomedical applications [39].

**3. Physical characteristics of magnetosomes**

*Biology and Physics of Magnetotactic Bacteria DOI: http://dx.doi.org/10.5772/intechopen.79965*

to the cytoskeletal filaments [47].

and electron diffraction [52].

**9**


#### **Table 1.**

*Proteins encoded by genes within* mamAB *operon in* Magnetospirillum *and their function.*

in the *mamAB* operon are sufficient for magnetosome biomineralization [30]. Examples of genes found in this operon and their functions are listed in **Table 1**. Interestingly, the transference of genes from the *mamAB* operon from *M. gryphiswaldense* strain MSR-1 to *Rhodospirillum rubrum* resulted in magnetite magnetosome production within the photosynthetic cell [39]. Because of the magnetic properties of magnetosomes, which will be discussed on the following topic, these nanometric magnetic structures have great importance for the development of new applications and processes in Biotechnology. However, one of the limitations of their use in biotechnological applications is the fastidiousness of MTB, which makes the production of magnetosomes in bioreactors expensive and with low yield. The transference of the ability to synthesize magnetosomes from MTB to

**Protein Function Effect on cell upon deletion Reference/**

magnetosomes

response

orientation

magnetic response

magnetic response

than <20 nm; cells without magnetic response

Decrease in magnetosome number and size; less efficient magnetic

Magnetosomes are not produced; no

Magnetosomes are not aligned in chains; reduced magnetic

Alignment of the magnetosomes in short chains and decrease in the number of magnetosomes

Increase in the formation of polycrystalline particles of magnetite; formation of crystals of hematite; no magnetic response

cells without magnetic response

magnetosomes; less efficient magnetic response

magnetosomes; less efficient magnetic response

Magnetosomes are not produced; no

MamA Activation of biomineralization Decrease in the number of

MamE Crystal maturation Synthesis of magnetosomes smaller

MamO Nucleation of the magnetite crystal Magnetosomes are not produced;

Magnetite crystal size control Decrease in the size of

*Proteins encoded by genes within* mamAB *operon in* Magnetospirillum *and their function.*

MamU Possibly lipid metabolism No changes were observed [29] Strain

MamP Magnetite crystal size control Decrease in the size of

MamB Transport of iron into the

*Microorganisms*

PDZ domains (MamE)

MamH Balance in the redox state of iron on the magnetosome membrane

MamJ Alignment of the magnetosome chain: it interacts with the surface of the magnetosome and with a structure similar to the cytoskeleton (MamK

MamK Controls the assembly, segregation, and positioning of the magnetosome

> magnetosome: magnetite nucleation, crystal growth, and stabilization of

chain inside the cell

MamM Transport of iron into the

MamI Synthesis of the magnetosome membrane

filament)

MamB

MamR MamT

**Table 1.**

**8**

magnetosome vesicle; interacts with

**strain used on the study**

[31] Strain AMB-1

[29] Strain AMB-1; [32] strain MSR-1

[29, 33] Strain AMB-1

[29] Strain AMB-1; [34] strain MSR-1

[29] Strain AMB-1

[35] Strain MSR-1

[36] Strain MSR-1

[29] Strain AMB-1; [32] strain MSR-1

[29] Strain AMB-1; [37] strain MSR-1

[29, 38] Strain AMB-1

[29, 38] Strain AMB-1

AMB-1

other cells represents a new frontier in Microbiology and greatly expands the use of magnetosomes in nanotechnological and biomedical applications [39].
