A contractile injection system stimulates tubeworm metamorphosis by translocating a proteinaceous effector

• Published in: eLife Vol. 8
• Main Authors: Ericson, Charles F, Eisenstein, Fabian, Medeiros, João M, Malter, Kyle E, Cavalcanti, Giselle S, Zeller, Robert W, Newman, Dianne K, Pilhofer, Martin, Shikuma, Nicholas J
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 17-09-2019; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Animal behavior; Animals; Bacteria; Bacterial Proteins - metabolism; Biochemistry; Biofilms; Biology; Biophysics; Biotechnology; Cells (Biology); contractile injection system; Contractility; Coral reefs; Corals; Cryoelectron Microscopy; development; Ecosystems; Electron Microscope Tomography; Environmental aspects; Genes; Genetic research; Genomics; Genotype & phenotype; Host Microbial Interactions; Injection systems; Life cycles; Marine animals; Marine bacteria; Marine biology; Marine ecosystems; Marine organisms; Mass spectrometry; Metamorphosis; Metamorphosis (Biology); Metamorphosis, Biological; Microbiology and Infectious Disease; Novels; Ocean bottom; Ocean floor; Oysters; phage; Phages; Physiological aspects; Polychaeta - drug effects; Polychaeta - growth & development; Polychaeta - microbiology; Protein Transport; Proteins; Pseudoalteromonas - metabolism; Reefs; Scientific imaging; Short Report; Structural Biology and Molecular Biophysics; Swimming; symbiosis; T6SS; Tomography; Tubeworms; Zoological research; United States; United States > US; California; development; T6SS; infectious disease; symbiosis; microbiology; structural biology; metamorphosis; molecular biophysics; phage; contractile injection system
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/elife.46845

The swimming larvae of many marine animals identify a location on the sea floor to undergo metamorphosis based on the presence of specific bacteria. Although this microbe-animal interaction is critical for the life cycles of diverse marine animals, what types of biochemical cues from bacteria that induce metamorphosis has been a mystery. Metamorphosis of larvae of the tubeworm
is induced by arrays of phage tail-like contractile injection systems, which are released by the bacterium
. Here we identify the novel effector protein Mif1. By cryo-electron tomography imaging and functional assays, we observe Mif1 as cargo inside the tube lumen of the contractile injection system and show that the
gene is required for inducing metamorphosis. Purified Mif1 is sufficient for triggering metamorphosis when electroporated into tubeworm larvae. Our results indicate that the delivery of protein effectors by contractile injection systems may orchestrate microbe-animal interactions in diverse contexts.