Structure of a thylakoid-anchored contractile injection system in multicellular cyanobacteria

• Published in: Nature microbiology Vol. 7; no. 3; pp. 386 - 396
• Main Authors: Weiss, Gregor L., Eisenstein, Fabian, Kieninger, Ann-Katrin, Xu, Jingwei, Minas, Hannah A., Gerber, Milena, Feldmüller, Miki, Maldener, Iris, Forchhammer, Karl, Pilhofer, Martin
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.03.2022; Nature Publishing Group
• Subjects: 14/19; 14/28; 14/34; 14/35; 14/63; 631/326/88; 631/535/1258/1259; 631/535/1258/1260; Anabaena; Apoptosis; Biomedical and Life Sciences; Cell death; Cell interactions; Contractility; Cryoelectron Microscopy; Cyanobacteria; Cyanobacteria - metabolism; Cytoplasmic membranes; Electron Microscope Tomography; Electron microscopy; Infectious Diseases; Injection systems; Life Sciences; Localization; Medical Microbiology; Microbiology; Parasitology; Phages; Thylakoids - metabolism; Type VI Secretion Systems - metabolism; Virology
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-021-01055-y

Contractile injection systems (CISs) mediate cell–cell interactions by phage tail-like structures, using two distinct modes of action: extracellular CISs are released into the medium, while type 6 secretion systems (T6SSs) are attached to the cytoplasmic membrane and function upon cell–cell contact. Here, we characterized a CIS in the multicellular cyanobacterium Anabaena , with features distinct from extracellular CISs and T6SSs. Cryo-electron tomography of focused ion beam-milled cells revealed that CISs were anchored in thylakoid membrane stacks, facing the cell periphery. Single particle cryo-electron microscopy showed that this unique in situ localization was mediated by extensions of tail fibre and baseplate components. On stress, cyanobacteria induced the formation of ghost cells, presenting thylakoid-anchored CISs to the environment. Functional assays suggest that these CISs may mediate ghost cell formation and/or interactions of ghost cells with other organisms. Collectively, these data provide a framework for understanding the evolutionary re-engineering of CISs and potential roles of these CISs in cyanobacterial programmed cell death. The characterization of a contractile injection system anchored in the thylakoid membrane of Anabaena reveals structural features linked to the unique localization and function of this cyanobacterial nanomachine.