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Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling

Shikuma, Nicholas J. and Antoshechkin, Igor and Medeiros, João M. and Pilhofer, Martin and Newman, Dianne K. (2016) Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling. Proceedings of the National Academy of Sciences of the United States of America, 113 (36). pp. 10097-10102. ISSN 0027-8424. PMCID PMC5018781. http://resolver.caltech.edu/CaltechAUTHORS:20160823-074209373

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Abstract

Diverse animal taxa metamorphose between larval and juvenile phases in response to bacteria. Although bacteria-induced metamorphosis is widespread among metazoans, little is known about the molecular changes that occur in the animal upon stimulation by bacteria. Larvae of the tubeworm Hydroides elegans metamorphose in response to surface-bound Pseudoalteromonas luteoviolacea bacteria, producing ordered arrays of phage tail-like metamorphosis-associated contractile structures (MACs). Sequencing the Hydroides genome and transcripts during five developmental stages revealed that MACs induce the regulation of groups of genes important for tissue remodeling, innate immunity, and mitogen-activated protein kinase (MAPK) signaling. Using two MAC mutations that block P. luteoviolacea from inducing settlement or metamorphosis and three MAPK inhibitors, we established a sequence of bacteria-induced metamorphic events: MACs induce larval settlement; then, particular properties of MACs encoded by a specific locus in P. luteoviolacea initiate cilia loss and activate metamorphosis-associated transcription; finally, signaling through p38 and c-Jun N-terminal kinase (JNK) MAPK pathways alters gene expression and leads to morphological changes upon initiation of metamorphosis. Our results reveal that the intricate interaction between Hydroides and P. luteoviolacea can be dissected using genomic, genetic, and pharmacological tools. Hydroides' dependency on bacteria for metamorphosis highlights the importance of external stimuli to orchestrate animal development. The conservation of Hydroides genome content with distantly related deuterostomes (urchins, sea squirts, and humans) suggests that mechanisms of bacteria-induced metamorphosis in Hydroides may have conserved features in diverse animals. As a major biofouling agent, insight into the triggers of Hydroides metamorphosis might lead to practical strategies for fouling control.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1603142113DOIArticle
http://www.pnas.org/content/113/36/10097PublisherArticle
http://www.pnas.org/content/113/36/10097/suppl/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5018781/PubMed CentralArticle
ORCID:
AuthorORCID
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2016 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Linda Z. Holland, University of California, San Diego, La Jolla, CA, and accepted by Editorial Board Member Nancy Knowlton July 13, 2016 (received for review February 24, 2016). Published online before print August 22, 2016. We thank Heather Maughan for providing constructive feedback and editing the manuscript. The authors acknowledge support from Piotr Szwedziak, Peter Tittmann, and ScopeM at ETH Zürich. Experiments were carried out in the laboratories of N.J.S., M.P., D.K.N., and at the Millard and Muriel Jacobs Genome Facility at Caltech. This work was supported by grants from the Office of Naval Research (N00014-14-1-0340 to N.J.S. and D.K.N.; N00014-16-1-2135 to N.J.S.), Swiss National Science Foundation (31003A_152878 to M.P.), ETH Zürich (ETH-45 15-1 to M.P.), and the Helmut Horten Foundation (to M.P.). N.J.S. and I.A. contributed equally to this work. Author contributions: N.J.S., I.A., J.M.M., M.P., and D.K.N. designed research; N.J.S., I.A., and J.M.M. performed research; N.J.S., I.A., J.M.M., M.P., and D.K.N. analyzed data; and N.J.S., I.A., and D.K.N. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. L.Z.H. is a Guest Editor invited by the Editorial Board. Data deposition: The raw sequence reads reported in this paper have been deposited in the National Center for Biotechnology Information Sequence Read Archive (SRA) database [accession nos. SRP067980 (genome) and SRP067899 (transcriptome)]. The whole-genome shotgun project reported in this paper has been deposited in the DNA Data Bank of Japan (DDBJ)/European Molecular Biology Laboratory (EMBL)/GenBank database (accession no. LQRL00000000, version LQRL01000000). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1603142113/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Office of Naval Research (ONR)N00014-14-1-0340
Office of Naval Research (ONR)N00014-16-1-2135
Swiss National Science Foundation (SNSF)31003A_152878
ETH ZürichETH-45 15-1
Helmut Horten FoundationUNSPECIFIED
Subject Keywords:genome; phage; symbiosis; biofouling; development
PubMed Central ID:PMC5018781
Record Number:CaltechAUTHORS:20160823-074209373
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160823-074209373
Official Citation:Nicholas J. Shikuma, Igor Antoshechkin, João M. Medeiros, Martin Pilhofer, and Dianne K. Newman Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling PNAS 2016 113 (36) 10097-10102; published ahead of print August 22, 2016, doi:10.1073/pnas.1603142113
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:69827
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Aug 2016 17:31
Last Modified:24 Oct 2017 16:45

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