Three-dimensional reconstruction of Magnetofaba australis strain IT-1: Magnetosome chain position with respect to flagella

Magnetotactic bacteria (MTB) form a distinct group encompassing morphologically, phylogenetically, and physiologically different microorganisms (Bazylinski and Frankel, 2004, Schüler, 2008). The locations where they can be found also differ significantly, being seen all over the globe in fresh and saltwater; some of them have been reported even in extreme environments (Bazylinski and Lefèvre, 2013, Lin et al., 2013, Lin et al., 2014). To this date, only flagellated aquatic Gram-negative prokaryotes have been observed, and their morphologies vary from rods, vibrio, cocci, and spirilla to multicellular forms denominated multicellular magnetotactic prokaryotes (Faivre and Schuler, 2008, Araujo et al., 2015). Despite the many differences, all of them can biomineralize the same organelle called magnetosome (Balkwill et al., 1980, Faivre and Schuler, 2008). Magnetosomes are composed of a mineral part, which can be a magnetic nanocrystal of magnetite (Fe3O4) or greigite (Fe3S4), and an organic part, the membranous envelope, encompassing the nanocrystal (Lefèvre et al., 2011). Some MTB are reported to biomineralize both magnetite and greigite simultaneously (Bazylinski et al., 1995; Faivre & Schüler, 2008).

Magnetosomes are arranged intracellularly in one or more chains that produce a magnetic moment in the cell (Spormann and Wolfe, 1984, Frankel et al., 1997). This permits a passive orientation with the geomagnetic field lines (GML) through a magnetic torque and allows magneto-aerotaxis, a phenomenon that occurs when an MTB passively orientated to the GML is propelled to swim by the flagellar apparatus and ends up swimming aligned to the GML. (Spormann and Wolfe, 1984, Frankel et al., 1997, Bazylinski and Frankel, 2004, Zhang and Wu, 2020).

MTB are microaerophilic and anaerobic and live in a chemically stratified environment that is constantly changing. Therefore, it is commonly acknowledged that magnetotaxis assists other taxes found in MTB, such as chemotaxis and aerotaxis (Bazylinski and Frankel, 2004, Frankel et al., 2007, Simmons et al., 2004, Lefèvre et al., 2014, Pfeiffer et al., 2021). So, the search for the oxic-anoxic interface (OAI) region, which is required for MTB survival, is optimized (Bazylinski and Frankel, 2004, Simmons et al., 2004, Komeili, 2012, Lefèvre et al., 2014, Mao et al., 2022). Magneto-aerotaxis can be explained by a classical model based on elongated cells as vibrio and rods, where the magnetosome chain(s) and, consequently, the magnetic moment are aligned with the longest axis of the MTB cells, which coincide with the swimming axis and flagellar apparatus (Spormann and Wolfe, 1984, Frankel et al., 1997, Lefèvre et al., 2014, Pfeiffer et al., 2021). So, when these MTB are aligned to the GML, they can be in two different states, oxidized or reduced (Spormann and Wolfe, 1984, Frankel et al., 1997). If MTB from the North Hemisphere find themselves in an oxidized state when aligned to the GML, they rotate their flagella counter-clockwise and move downward in the stratified environment seeking the OAI; the inverse occurs when MTB is in a reduced state; they rotate clockwise their flagella and moves upward to a more oxidized region. The same happens with MTB in the South Hemisphere (Spormann and Wolfe, 1984, Frankel et al., 1997, Simmons et al., 2006). Therefore, the classical model facilitates understanding magneto-aerotaxis and motility behavior in MTB with elongated morphologies. (Spormann and Wolfe, 1984, Frankel et al., 1997, Bazylinski and Frankel, 2004).

However, MTB is a diversified group, and more than one model based on a specified morphology, like the classical model, can hinder understanding motility behavior. The difficulty of cultivating MTB could explain the absence of new axenic cultures and, consequently, other models that could clarify magneto-aerotaxis as axenic cultures are essential to studying magneto-aerotaxis and its influence on the motility behavior of the cell studied. Until recently, cocci morphology was the most often observed in environmental samples, and their morphology differs of elongated cells, which makes it challenging to understand magneto-aerotaxis and its advantages in cells with this morphology when only using the classical model as reference.

Our group previously isolated and cultivated a new MTB from the Etaproteobacteria class based on the 16S rRNA gene sequence, denominated Magnetofaba australis strain IT-1. It was the first axenic culture of an MTB isolated from the Southern Hemisphere (Itaipu Lagoon in Rio de Janeiro, Brazil) and the first cocci MTB reported with elongated cuboctahedric morphology in their magnetosomes(Morillo et al., 2014). In subsequent studies, some peculiarities in the motility behavior of Mf. australis strain IT-1, such as the form they swim with the flagellar apparatus pulling the cell to the direction of movement instead of pushing the cell. These MTB do not seem to fit the classical model to explain magneto-aerotaxis (Araujo et al., 2016). Due to its motility behavior and the spatial disposition of their sole chain of magnetosomes, the simple act of rotating the flagella to move would lead to a misalignment of the bacterial magnetic moment with the GML and impending the magneto-aerotaxis to occur correctly (Araujo et al., 2016). However, despite these peculiarities, Mf. australis strain IT-1 can swim at high speeds while aligned with the GML (Araujo et al., 2016). Thus, this bacterium is an excellent choice for studying magneto-aerotaxis in MTB of morphologies that are not easily in line with the classical model, given that this MTB has an apparent conflict with it.

In the present study, we observe the spatial disposition of magnetosomes, motility behavior, resistance to reactive oxygen species (ROS), and the influence of magneto-aerotaxis in Mf. australis strain IT-1. This bacterium has a coccoid/ovoid morphology with cuboctahedric elongated magnetosomes of magnetite; it can achieve high swimming speeds such as 300 µm.s−1 and has some peculiarity in the way it swims where the flagellar apparatus pulls the cell to the direction of movement instead of pushing the cell to the direction of movement (Araujo et al., 2016).

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