Positioning the Flagellum at the Center of a Dividing Cell To Combine Bacterial Division with Magnetic Polarity

Abstract

ABSTRACT Faithful replication of all structural features is a sine qua non condition for the success of bacterial reproduction by binary fission. For some species, a key challenge is to replicate and organize structures with multiple polarities. Polarly flagellated magnetotactic bacteria are the prime example of organisms dealing with such a dichotomy; they have the challenge of bequeathing two types of polarities to their daughter cells: magnetic and flagellar polarities. Indeed, these microorganisms align and move in the Earth's magnetic field using an intracellular chain of nano-magnets that imparts a magnetic dipole to the cell. The paradox is that, after division occurs in cells, if the new flagellum is positioned opposite to the old pole devoid of a flagellum during cell division, the two daughter cells will have opposite magnetic polarities with respect to the positions of their flagella. Here we show that magnetotactic bacteria of the class Gammaproteobacteria pragmatically solve this problem by synthesizing a new flagellum at the division site. In addition, we model this particular structural inheritance during cell division. This finding opens up new questions regarding the molecular aspects of the new division mechanism, the way other polarly flagellated magnetotactic bacteria control the rotational direction of their flagella, and the positioning of organelles. IMPORTANCE Magnetotactic bacteria produce chains of magnetic nanoparticles that endow the cells with a magnetic dipole, a “compass” used for navigation. This feature, however, also drastically complicates cellular division in the case of polarly flagellated bacteria. In this case, the bacteria have to pass on to their daughter cells two types of cellular polarities simultaneously, their magnetic polarity and the polarity of their motility apparatus. We show here that magnetotactic bacteria of the Gammaproteobacteria class pragmatically solve this problem by synthesizing the new flagellum at the division site, a division scheme never observed so far in bacteria. Even though the molecular mechanisms behind this scheme cannot be resolved at the moment due to the lack of genetic tools, this discovery provides a new window into the organizational complexity of simple organisms.