Structure and Function of a Bacterial Gap Junction Analog

• Published in: Cell Vol. 178; no. 2; pp. 374 - 384.e15
• Main Authors: Weiss, Gregor L., Kieninger, Ann-Katrin, Maldener, Iris, Forchhammer, Karl, Pilhofer, Martin
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 11.07.2019; Cell Press
• Subjects: Anabaena - metabolism; Bacterial Proteins - chemistry; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Carbonyl Cyanide m-Chlorophenyl Hydrazone - analogs & derivatives; Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology; Cell Communication - drug effects; cell-cell connections; Cryoelectron Microscopy; cyanobacteria; electron cryotomography; fluorescence recovery after photobleaching; Gap Junctions - chemistry; Gap Junctions - metabolism; Gap Junctions - ultrastructure; Membrane Proteins - chemistry; Membrane Proteins - genetics; Membrane Proteins - metabolism; membrane trafficking; multicellularity; Mutagenesis; septal junctions; subtomogram averaging; multicellularity; cyanobacteria; cell-cell connections; septal junctions; subtomogram averaging; membrane trafficking; electron cryotomography; fluorescence recovery after photobleaching
• ISSN: 0092-8674; 1097-4172; 1097-4172
• DOI: 10.1016/j.cell.2019.05.055

Multicellular lifestyle requires cell-cell connections. In multicellular cyanobacteria, septal junctions enable molecular exchange between sister cells and are required for cellular differentiation. The structure of septal junctions is poorly understood, and it is unknown whether they are capable of controlling intercellular communication. Here, we resolved the in situ architecture of septal junctions by electron cryotomography of cryo-focused ion beam-milled cyanobacterial filaments. Septal junctions consisted of a tube traversing the septal peptidoglycan. Each tube end comprised a FraD-containing plug, which was covered by a cytoplasmic cap. Fluorescence recovery after photobleaching showed that intercellular communication was blocked upon stress. Gating was accompanied by a reversible conformational change of the septal junction cap. We provide the mechanistic framework for a cell junction that predates eukaryotic gap junctions by a billion years. The conservation of a gated dynamic mechanism across different domains of life emphasizes the importance of controlling molecular exchange in multicellular organisms. [Display omitted] •The in situ architecture of septal junctions reveals cap, plug, and tube modules•Septal junctions reversibly control cell-cell communication upon stress•FraD is a structural element of the septal junction plug module•Bacterial septal junctions are mechanistically analogous to metazoan gap junctions The in situ architecture of cyanobacterial septal junctions reveals a gated intercellular communication channel that evolutionarily predates eukaryotic gap junctions by a billion years.