Diacylglycerol, PKC and MAPK signaling initiate tubeworm metamorphosis in response to bacteria

• Published in: Developmental biology Vol. 487; pp. 99 - 109
• Main Authors: Malter, Kyle E., Esmerode, Milagros, Damba, Myedith, Alker, Amanda T., Forsberg, Erica M., Shikuma, Nicholas J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-07-2022
• Subjects: Animals; Diglycerides; Larva; Metamorphosis, Biological; Mitogen-Activated Protein Kinases; Polychaeta; Protein Kinase C; Signal Transduction
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/j.ydbio.2022.04.009

External environmental cues can have significant impacts on the timing and outcomes of animal development. For the swimming larvae of many marine invertebrates, the presence of specific surface-bound bacteria are important cues that help larvae identify a suitable location on the sea floor for metamorphosis and adult life. While metamorphosis in response to bacteria occurs in diverse animals from across the animal tree of life, we know little about the signal transduction cascades stimulated at the onset of metamorphosis upon their interaction with bacteria. The metamorphosis of a model tubeworm, Hydroides elegans, is triggered by the bacterium Pseudoalteromonas luteoviolacea which produces a stimulatory protein called Mif1. In this work, we define three key nodes in a signaling cascade promoting Hydroides metamorphosis in response to Mif1. Using metabolomic profiling, we find that the stimulation of Hydroides larvae by P. luteoviolacea leads to an increase in diacylglycerol during the initiation of metamorphosis, and that Mif1 is necessary for this upregulation. Genomic and pharmacological examination suggests that diacylglycerol triggers a phosphotransferase signaling cascade involving Protein Kinase C (PKC) and Mitogen-Activated Protein Kinase (MAPK), to induce Hydroides metamorphosis. Additionally, Mif1 activates the expression of two nuclear hormone receptors, HeNHR1 and HeNHR2 in the cerebral ganglia of Hydroides larvae. Our results define a post-translational signal transduction pathway mediating bacteria-stimulated metamorphosis in a model invertebrate animal.
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•Bacteria initiate tubeworm metamorphosis through post-translational signaling.•Lipidomics revealed an increase in diacylglycerol upon bacteria stimulation.•Diacylglycerol promotes Protein Kinase C, MAPK signaling to initiate metamorphosis.•Bacteria stimulate the expression of two nuclear hormone receptor genes in the larval cerebral ganglia.