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

• Published in: Environmental microbiology Vol. 22; no. 4; pp. 1481 - 1494
• Main Authors: Qian, Xin‐Xin, Santini, Claire‐Lise, Kosta, Artemis, Menguy, Nicolas, Le Guenno, Hugo, Zhang, Wenyan, Li, Jinhua, Chen, Yi‐Ran, Liu, Jia, Alberto, François, Espinosa, Leon, Xiao, Tian, Wu, Long‐Fei
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.04.2020; Wiley Subscription Services, Inc; Society for Applied Microbiology and Wiley-Blackwell
• Subjects: Cell Adhesion; Cell Division; Cell Membrane; Cell surface; Cells; Confocal microscopy; Electron microscopy; Flagella; Fluorescence; Fluorescence in situ hybridization; Freezing; Geomagnetic field; Geomagnetism; Hybridization; In Situ Hybridization, Fluorescence; Life Sciences; Magnetic Phenomena; Membranes; Microscopy; Microscopy, Electron, Scanning; Offspring; Photokinesis; Prokaryotes; Prokaryotic Cells - physiology; Prokaryotic Cells - ultrastructure; Scanning electron microscopy; Structure-function relationships; Swimming
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.14710

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.