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Marine Tubeworm Metamorphosis Induced by Arrays of Bacterial Phage Tail–Like Structures

Shikuma, Nicholas J. and Pilhofer, Martin and Weiss, Gregor L. and Hadfield, Michael G. and Jensen, Grant J. and Newman, Dianne K. (2014) Marine Tubeworm Metamorphosis Induced by Arrays of Bacterial Phage Tail–Like Structures. Science, 343 (6170). pp. 529-533. ISSN 0036-8075. PMCID PMC4949041. doi:10.1126/science.1246794.

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Many benthic marine animal populations are established and maintained by free-swimming larvae that recognize cues from surface-bound bacteria to settle and metamorphose. Larvae of the tubeworm Hydroides elegans, a significant biofouling agent, require contact with surface-bound bacteria to undergo metamorphosis; however, the mechanisms that underpin this microbially mediated developmental transition have been enigmatic. Here, we show that a marine bacterium, Pseudoalteromonas luteoviolacea, produces arrays of phage tail–like structures that trigger metamorphosis of H. elegans. These arrays comprise about 100 contractile structures with outward-facing baseplates, linked by tail fibers and a dynamic hexagonal net. Not only do these arrays suggest a novel form of bacterium-animal interaction, they provide an entry point to understanding how marine biofilms can trigger animal development.

Item Type:Article
Related URLs:
URLURL TypeDescription CentralArticle
Shikuma, Nicholas J.0000-0001-5518-5020
Jensen, Grant J.0000-0003-1556-4864
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2014 American Association for the Advancement of Science. Received 3 October 2013; accepted 23 December 2013. Published Online January 9 2014. We thank B. Pernet for help with locating and identifying tubeworms and for gifting the algal strain used in this work; A. McDowall for help with electron microscopy; Y. Huang, who created the Str^R-strain (7); A. Asahina and S. Wilbur for laboratory assistance; J. Levine for help with timelapse microscopy; J. Ricci for help with phylogenetic analyses; and members of the Newman group for discussions and comments on the manuscript. The Howard Hughes Medical Institute, Z. Yu and J. de la Cruz are acknowledged for providing access to the FEI Titan Krios at Janelia Farm and support in data collection. N.J.S. was supported by a Caltech Division of Biology Postdoctoral Fellowship. This collaboration was supported by the Caltech Center for Environmental Microbiology Interactions, the Howard Hughes Medical Institute (D.K.N. and G.J.J.), Office of Naval Research grants N00014-08-1-0413 and N00014-05-1-0579 (M.G.H.), NIH grant GM094800B (G.J.J.), and a gift from the Gordon and Betty Moore Foundation (Caltech). D.K.N. and G.J.J. are Investigators of the Howard Hughes Medical Institute. Strains obtained from the American Type Culture Collection listed in table S2 (ATCC 33492, ATCC 14393, ATCC 15057). DNA sequences encoding for mac, T6SS, and bacteriocin-2 genes are deposited under GenBank accession numbers KF724687, KF724688, and KF724689, respectively. Subtomogram averages were deposited in the Electron Microscopy Data Bank (accession numbers to be added on proof). Author contributions: All authors designed research. N.J.S., M.P. and G.L.W. performed research. All authors wrote the paper.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funding AgencyGrant Number
Caltech Division of Biology Postdoctoral FellowshipUNSPECIFIED
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Office of Naval Research (ONR)N00014-08-1-0413
Office of Naval Research (ONR)N00014-05-1-0579
Gordon and Betty Moore FoundationUNSPECIFIED
Issue or Number:6170
PubMed Central ID:PMC4949041
Record Number:CaltechAUTHORS:20140113-134430398
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:43345
Deposited By: Tony Diaz
Deposited On:15 Jan 2014 00:04
Last Modified:10 Nov 2021 16:36

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