Marine Tubeworm Metamorphosis Induced by Arrays of Bacterial Phage Tail–Like Structures
Big MACs
Tubeworms are important marine benthic species that encrust rocks and contribute to fouling of man-made objects, such as ships' hulls and drilling well heads. Like most marine invertebrates, the larval stages of tubeworms are free-swimming, but the cues for larval settlement and the triggers for metamorphosis are mysterious. Shikuma et al. (p. 529, published online 9 January) experimented on larval settlement by the tubeworm, Hydroides elegans, which needs to associate with a biofilm-forming bacterium, Pseudoalteromonas luteoviolacea, before settlement can occur. The bacterium was found to express metamorphosis-associated contractile structures (MACs) in large and structurally elaborate arrays that allow the tubeworm larvae to develop.
Abstract
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, an important 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.
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Supplementary Material
Summary
Materials and Methods
Figs. S1 to S10
Tables S1 to S4
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Volume 343 | Issue 6170
31 January 2014
31 January 2014
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Copyright © 2014, American Association for the Advancement of Science.
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Received: 3 October 2013
Accepted: 23 December 2013
Published in print: 31 January 2014
Acknowledgments
We thank B. Pernet for help with locating and identifying tubeworms and for giving us the algal strain used in this work; A. McDowall for help with EM; Y. Huang, who created the StrR-strain (7); A. Asahina and S. Wilbur for laboratory assistance; J. Levine for help with time-lapse 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 California Institute of Technology (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 EMD-2543, EMD-2544, and EMD-2545). Author contributions: All authors designed research. N.J.S., M.P. and G.L.W. performed research. All authors wrote the paper.
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