Stepwise metamorphosis of the tubewormHydroides elegansis 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 tubewormHydroides elegansmetamorphose in response to surface-boundPseudoalteromonas luteoviolaceabacteria, producing ordered arrays of phage tail-like metamorphosis-associated contractile structures (MACs). Sequencing theHydroidesgenome 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 blockP. luteoviolaceafrom 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 inP. luteoviolaceainitiate 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 betweenHydroidesandP. luteoviolaceacan 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 ofHydroidesgenome content with distantly related deuterostomes (urchins, sea squirts, and humans) suggests that mechanisms of bacteria-induced metamorphosis inHydroidesmay have conserved features in diverse animals. As a major biofouling agent, insight into the triggers ofHydroidesmetamorphosis might lead to practical strategies for fouling control.