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

Ericson, Charles F. and Eisenstein, Fabian and Medeiros, João M. and Malter, Kyle E. and Cavalcanti, Giselle S. and Zeller, Robert W. and Newman, Dianne K. and Pilhofer, Martin and Shikuma, Nicholas J. (2019) A contractile injection system stimulates tubeworm metamorphosis by translocating a proteinaceous effector. eLife, 8 . Art. No. e46845. ISSN 2050-084X. PMCID PMC6748791. https://resolver.caltech.edu/CaltechAUTHORS:20190923-092135402

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Abstract

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 Hydroides elegans is induced by arrays of phage tail-like contractile injection systems, which are released by the bacterium Pseudoalteromonas luteoviolacea. 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 mif1 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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/elife.46845DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6748791PubMed CentralArticle
https://www.ebi.ac.uk/pdbe/entry/emdb/EMD-4730Related ItemID EMD-4730. Subtomogram average of MAC sheath and inner tube of P. luteoviolacea Mif1 mutant
https://www.ebi.ac.uk/pdbe/entry/emdb/EMD-4731Related ItemID EMD-4731. Subtomogram average of MAC sheath and inner tube of wildtype P. luteoviolacea
ORCID:
AuthorORCID
Ericson, Charles F.0000-0002-2854-0696
Medeiros, João M.0000-0001-9075-548X
Malter, Kyle E.0000-0002-3056-8751
Newman, Dianne K.0000-0003-1647-1918
Shikuma, Nicholas J.0000-0001-5518-5020
Additional Information:© 2019 Ericson et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 14 March 2019; Accepted: 05 August 2019; Published: 17 September 2019. We thank Dr. Anca Segall and Dr. Manal Swairjo for reagents, technical support and constructive suggestions. We thank Ms. Amanda Alker and Ms. Nathalie Delherbe for their constructive suggestions. ScopeM at ETHZ and Ohad Medalia at the University of Zürich are acknowledged for instrument access. We thank Paula Picotti and Marco Faini for discussions of mass spectrometry experiments. This work was supported by the Harold and June Memorial Scholarship (CFE), Norma Sullivan Memorial Endowed Scholarship (CFE), Howard Hughes Medical Institute (DKN), NIH NIDCD (1R21DC013180-01A1, RWZ), Office of Naval Research (N00014-17-1-2677, NJS and SB), Office of Naval Research (N00014-16-1-2135, NJS), Office of Naval Research (N00014-14-1-0340, NJS and DKN), Alfred P Sloan Foundation, Sloan Research Fellowship (NJS), San Diego State University (NJS), European Research Council (679209, MP), Swiss National Science Foundation (31003A_179255, MP) and Gebert Rüf Foundation (MP). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Author contributions: Charles F Ericson, Kyle E Malter, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing; Fabian Eisenstein, João M Medeiros, Formal analysis, Investigation, Visualization, Methodology, Writing—review and editing; Giselle S Cavalcanti, Investigation, Writing—review and editing; Robert W Zeller, Resources, Funding acquisition, Methodology, Writing—review and editing; Dianne K Newman, Conceptualization, Resources, Supervision, Funding acquisition, Validation, Project administration, Writing—review and editing; Martin Pilhofer, Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing; Nicholas J Shikuma, Conceptualization, Resources, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing. Data availability: Subtomogram averages were deposited in the Electron Microscopy Data Bank (accession numbers EMD-4730 and EMD-4731).
Funders:
Funding AgencyGrant Number
Harold and June Memorial ScholarshipUNSPECIFIED
Norma Sullivan Memorial Endowed ScholarshipUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NIH1R21DC013180-01A1
Office of Naval Research (ONR)N00014-17-1-2677
Office of Naval Research (ONR)N00014-16-1-2135
Office of Naval Research (ONR)N00014-14-1-0340
Alfred P Sloan FoundationUNSPECIFIED
San Diego State UniversityUNSPECIFIED
European Research Council (ERC)679209
Swiss National Science Foundation (SNSF)31003A_179255
Gebert Rüf FoundationUNSPECIFIED
PubMed Central ID:PMC6748791
Record Number:CaltechAUTHORS:20190923-092135402
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190923-092135402
Official Citation:Ericson, Charles F et al. “A contractile injection system stimulates tubeworm metamorphosis by translocating a proteinaceous effector.” eLife vol. 8 e46845. 17 Sep. 2019, doi:10.7554/eLife.46845
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:98789
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Sep 2019 16:37
Last Modified:29 Oct 2019 20:32

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