title: Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling.
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.
authors.affiliation: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; nshikuma@mail.sdsu.edu.
authors.forename: Nicholas J
authors.initials: NJ
authors.lastname: Shikuma
authors.affiliation: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125;
authors.forename: Igor
authors.initials: I
authors.lastname: Antoshechkin
authors.affiliation: Institute of Molecular Biology and Biophysics, Department of Biology, Eidgenössische Technische Hochschule Zürich, 8093 Zürich, Switzerland;
authors.forename: João M
authors.initials: JM
authors.lastname: Medeiros
authors.affiliation: Institute of Molecular Biology and Biophysics, Department of Biology, Eidgenössische Technische Hochschule Zürich, 8093 Zürich, Switzerland;
authors.forename: Martin
authors.initials: M
authors.lastname: Pilhofer
authors.affiliation: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125.
authors.forename: Dianne K
authors.initials: DK
authors.lastname: Newman
mesh_terms: D000818:Animals; D057219:Biofouling / Q000517:prevention & control; D002923:Cilia / Q000235:genetics / Q000276:immunology / Q000382:microbiology; D018507:Gene Expression Regulation, Developmental; D016678:Genome; D007113:Immunity, Innate; D048031:JNK Mitogen-Activated Protein Kinases / Q000235:genetics / Q000276:immunology; D008675:Metamorphosis, Biological / Q000235:genetics* / Q000276:immunology; D011077:Polychaeta / Q000235:genetics* / Q000254:growth & development / Q000276:immunology / Q000382:microbiology; D047428:Protein Kinase Inhibitors / Q000494:pharmacology; D031161:Pseudoalteromonas / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000276:immunology; D015398:Signal Transduction; D013559:Symbiosis / Q000235:genetics*; D014561:Urochordata / Q000235:genetics / Q000254:growth & development; D048051:p38 Mitogen-Activated Protein Kinases / Q000235:genetics* / Q000276:immunology
chemical_list: D047428:Protein Kinase Inhibitors; D012333:RNA, Messenger; D048031:JNK Mitogen-Activated Protein Kinases; D048051:p38 Mitogen-Activated Protein Kinases
keywords: biofouling; development; genome; phage; symbiosis