Bacterial lipopolysaccharide induces settlement and metamorphosis in a marine larva

Abstract

AbstractHow larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth and reproduction is an enduring question in marine science. Biofilm induced metamorphosis has been observed in marine invertebrate larvae from nearly every major marine phylum. Despite the widespread nature of this phenomenon the mechanism of induction remains poorly understood. The serpulid polychaete Hydroides elegans is a well-established model for investigating bacteria-induced larval development. A broad range of biofilm bacterial species elicit larval metamorphosis in H. elegans via at least two mechanisms, including outer membrane vesicles and phage-tail bacteriocins. We investigated the interaction between larvae of H. elegans and the inductive bacterium Cellulophaga lytica, which produces an abundance of OMVs but not phage-tail bacteriocins. We asked whether the OMVs of C. lytica induce larval settlement due to cell membrane components or through delivery of specific cargo. Employing a biochemical structure-function approach with a strong ecological focus, the cells and outer membrane vesicles produced by C. lytica were interrogated to determine the nature of the inductive molecule. Here we report that the cue produced by C. lytica that induces larvae of H. elegans to metamorphose is lipopolysaccharide (LPS). The widespread prevalence of LPS and its associated taxonomic and structural variability suggest it may be a broadly employed cue for bacterially induced larval settlement of marine invertebrates.Significance StatementNew surfaces in the sea are quickly populated by dense communities of invertebrate animals, whose establishment and maintenance require site-specific settlement of larvae from the plankton. Although it is recognized that larvae selectively settle in sites where they can metamorphose and thrive, and that the biofilm bacteria residing on these surfaces supply inductive cues, the nature of the cues used to identify ‘right places’ has remained enigmatic. In this paper, we reveal that lipopolysaccharide (LPS) from the outer membrane of a marine Gram-negative bacterium cue metamorphosis for a marine worm and discuss the likelihood that LPS provides the variation necessary to explain settlement site selectivity for many of the bottom-living invertebrate animals that metamorphose in response to bacterial biofilms.