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Summary Pseudoalteromonas luteoviolaceais a globally distributed marine bacterium that stimulates the metamorphosis of marine animal larvae, an important bacteria–animal interaction that can promote the recruitment of animals to benthic ecosystems. Recently, differentP.luteoviolaceaisolates have been shown to produce two stimulatory factors that can induce tubeworm and coral metamorphosis; Metamorphosis‐Associated Contractile structures (MACs) and tetrabromopyrrole (TBP) respectively. However, it remains unclear what proportion ofP.luteoviolaceaisolates possess the genes encoding MACs, and what phenotypic effect MACs and TBP have on other larval species. Here, we show that 9 of 19 sequencedP.luteoviolaceagenomes genetically encode both MACs and TBP. WhileP.luteoviolaceabiofilms producing MACs stimulate the metamorphosis of the tubewormHydroides elegans, TBP biosynthesis genes had no effect under the conditions tested. Although MACs are lethal to larvae of the cnidarianHydractinia symbiologicarpus,P.luteoviolaceamutants unable to produce MACs are capable of stimulating metamorphosis. Our findings reveal a hidden complexity of interactions between a single bacterial species, the factors it produces and two species of larvae belonging to different phyla.
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This content will become publicly available on December 27, 2025
A bacterial membrane-disrupting protein stimulates animal metamorphosis
ABSTRACT Diverse marine animals undergo a metamorphic larval-to-juvenile transition in response to surface-bound bacteria. Although this host-microbe interaction is critical to establishing and maintaining marine animal populations, the functional activity of bacterial products and how they activate the host’s metamorphosis program has not yet been defined for any animal. The marine bacteriumPseudoalteromonas luteoviolaceastimulates the metamorphosis of a tubeworm calledHydroides elegansby producing a molecular syringe called metamorphosis-associated contractile structures (MACs). MACs stimulate metamorphosis by injecting a protein effector termed metamorphosis-inducing factor 1 (Mif1) into tubeworm larvae. Here, we show that MACs bind to tubeworm cilia and form visible pores on the cilia membrane surface, which are smaller and less numerous in the absence of Mif1.In vitro, Mif1 associates with eukaryotic lipid membranes and possesses phospholipase activity. MACs can also deliver Mif1 to human cell lines and cause parallel phenotypes, including cell surface binding, membrane disruption, calcium flux, and mitogen-activated protein kinase activation. Finally, MACs can also stimulate metamorphosis by delivering two unrelated membrane-disrupting proteins, MLKL and RegIIIɑ. Our findings demonstrate that membrane disruption by MACs and Mif1 is necessary forHydroidesmetamorphosis, connecting the activity of a bacterial protein effector to the developmental transition of a marine animal. IMPORTANCEThis research describes a mechanism wherein a bacterium prompts the metamorphic development of an animal from larva to juvenile form by injecting a protein that disrupts membranes in the larval cilia. Specifically, results show that a bacterial contractile injection system and the protein effector it injects form pores in larval cilia, influencing critical signaling pathways like mitogen-activated protein kinase and calcium flux, ultimately driving animal metamorphosis. This discovery sheds light on how a bacterial protein effector exerts its activity through membrane disruption, a phenomenon observed in various bacterial toxins affecting cellular functions, and elicits a developmental response. This work reveals a potential strategy used by marine organisms to respond to microbial cues, which could inform efforts in coral reef restoration and biofouling prevention. The study’s insights into metamorphosis-associated contractile structures’ delivery of protein effectors to specific anatomical locations highlight prospects for future biomedical and environmental applications.
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- Award ID(s):
- 1942251
- PAR ID:
- 10566845
- Editor(s):
- Dubilier, Nicole
- Publisher / Repository:
- American Society for Microbiology
- Date Published:
- Journal Name:
- mBio
- ISSN:
- 2150-7511
- Subject(s) / Keyword(s):
- metamorphosis, contractile injection system, effector, pore-forming toxin, cilia, toxin, secretion systems
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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