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

Abstract

Summary 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.

Flagella and Swimming Behavior of Marine Magnetotactic Bacteria

“…The basal body also contains the flagellar protein export Phylogenetically, magnetotactic bacteria are members of several classes of the Proteobacteria phylum including the Alpha-, Gamma-, Delta-, Zeta-, Candidatus Lambda-, Candidatus Eta-classes, the Nitrospirae phylum, the Candidatus Omnitrophica phylum, the Candidatus Latescibacteria phylum, and the Planctomycetes phylum [7]. They present various morphotypes including cocci, spirilla, rod-shaped, vibrio, and more complex multicellular magnetotactic prokaryotes that are also called magnetoglobules (MMP) [1,8].…”

“…Since then, these types of magnetoglobules have been observed worldwide [36][37][38][39][40][41][42]. The second morphotype, the ellipsoidal or pineapple-like magnetoglobules, were observed in the Mediterranean Sea [8,43,44], the China Sea, and the Pacific Ocean [45][46][47][48][49]. Approximately 60 cells axisymmetrically assemble along the longitudinal axis to achieve a one-layer hollow entity that is held by a lattice at the surface [8].…”

“…The second morphotype, the ellipsoidal or pineapple-like magnetoglobules, were observed in the Mediterranean Sea [8,43,44], the China Sea, and the Pacific Ocean [45][46][47][48][49]. Approximately 60 cells axisymmetrically assemble along the longitudinal axis to achieve a one-layer hollow entity that is held by a lattice at the surface [8]. Phylogenetic studies have identified eleven species belonging to six genera of spherical magnetoglobules and nine species belonging to six genera of ellipsoidal magnetoglobules.…”

“…Phylogenetic studies have identified eleven species belonging to six genera of spherical magnetoglobules and nine species belonging to six genera of ellipsoidal magnetoglobules. They formed branches of a magnetoglobule clade, which are affiliated with Deltaproteobacteria, but are distinguished from another multicellular Deltaproteobacteria, the myxobacteria [8]. Both morphotypes exhibit a conspicuous periphery-core architecture.…”

“…The third group is the magnetoglobules that have developed both multicellular and magnetotactic properties during their evolution. To date, magnetotactic multicellular prokaryotes are found only in marine environments [8]. They exhibit peculiar patterns of motility by coordinatively rotating tens of thousands of peritrichous flagella (Figure 1, B), including both polar and axis magneto-aerotaxis, ping-pong motion, and photophobic and photokinesis swimming patterns.…”