Abstract
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.
Highlights
Bacteria evolved a variety of sophisticated macromolecular assemblies to translocate effectors into extracellular space or directly into target cells[1,2]
Anabaena Contractile injection systems (CISs) are anchored in thylakoid membrane stacks
We relabelled the genes with the prefix ‘cis’ and numbered them according to their homology to the close extracellular CISs (eCIS) relative antifeeding prophages (AFPs) (Fig. 1a and Supplementary Table 1)
Summary
Bacteria evolved a variety of sophisticated macromolecular assemblies to translocate effectors into extracellular space or directly into target cells[1,2]. Contractile injection systems (CISs) are a diverse, yet evolutionarily related, group of assemblies that mediate bacterial cell–cell interactions[3,4,5,6] Their contractile apparatus is homologous to contractile phage tails, using a contractile outer sheath to propel an effector-loaded tube into target cells. Several phylogenetically closely related CISs have recently been studied and are intriguing This group contains representatives of both eCISs and T6SSs. Characterized representatives are insecticidal eCISs such as antifeeding prophages (AFPs) and Photorhabdus virulence cassettes (PVCs), as well as large arrays of eCISs that induce the metamorphosis of tubeworm larvae (MACs)[10,11,12,13,14]. While 40% of sequenced cyanobacterial genomes contain at least one CIS gene cluster[16], their structure, mode of action and role in the cyanobacterial lifecycle remain unknown
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