Two Distinct Bacterial Biofilm Components Trigger Metamorphosis in the Colonial Hydrozoan Hydractinia echinata

Bacterial biofilms profoundly influence the recruitment and settlement of marine invertebrates, critical steps for diverse marine processes such as the formation of coral reefs, the maintenance of marine fisheries, and the fouling of submerged surfaces. However, the complex composition of biofilms often makes the characterization of individual signals and regulatory mechanisms challenging.

Diminished growth and vitality in juvenile Hydractinia echinata under anticipated future temperature and variable nutrient conditions

In a warming climate, rising seawater temperatures and declining primary and secondary production will drastically affect growth and fitness of marine invertebrates in the northern Atlantic Ocean. To study the ecological performance of juvenile hydroids Hydractinia echinata we exposed them to current and predicted water temperatures which reflect the conditions in the inter- and subtidal in combination with changing food availability (high and low) in laboratory experiments. Here we show, that the interplay between temperature stress and diminished nutrition affected growth and vitality of juvenile hydroids more than either factor alone, while high food availability mitigated their stress responses. Our numerical growth model indicated that the growth of juvenile hydroids at temperatures beyond their optimum is a saturation function of energy availability. We demonstrated that the combined effects of environmental stressors should be taken into consideration when evaluating consequences of climate change. Interactive effects of ocean warming, decreasing resource availability and increasing organismal energy demand may have major impacts on biodiversity and ecosystem function.

Two distinct bacterial biofilm components trigger metamorphosis in the colonial hydrozoan Hydractinia echinata

Bacterial-induced metamorphosis of larvae is a widespread cross-kingdom communication phenomenon within the marine environment and critical for the persistence of many invertebrate populations. However, the chemical structures of the majority of inducing bacterial signals and the underlying cellular mechanisms remain enigmatic. Hydractinia echinata larvae transform upon detection of bacterial biofilm components into the colonial adult stage. Despite serving as cell biological model system for decades, the inducing bacterial signals remained undiscovered. Using a chemical-ecology driven analysis, we herein identified that specific bacterial (lyso)phospholipids and polysaccharides, naturally present in bacterial biofilms, elicit metamorphosis in Hydractinia larvae. While (lyso)phospholipids (e.g. 16:0LPG/18:1LPE, 16:0 LPA/18:1LPE) as single compounds or in combinations induced up to 50% of all larvae to transform within 48 h, two structurally distinct polysaccharides, the newly identified Rha-Man polysaccharide from Pseudoalteromonas sp. P1-9 and curdlan from Alcaligenes faecalis caused up to 75% of all larvae to transform within 24 h. We also found combinations of (lyso)phospholipids and curdlan induced the transformation in almost all larvae within 24 h, thereby exceeding the morphogenic activity observed for single compounds and axenic bacterial biofilms. By using fluorescence-labeled bacterial phospholipids, we demonstrated their incorporation into the larval membranes, where interactions with internal signaling cascades could occur. Our results demonstrate that multiple and structurally distinct bacterial-derived metabolites converge to induce high transformation rates of Hydractinia larvae, which might ensure optimal habitat selection despite the general widespread occurrence of both compound classes.Significance StatementBacterial biofilms profoundly influence the recruitment and settlement of marine invertebrates, critical steps for diverse marine processes such as coral reef formation, marine fisheries and the fouling of submerged surfaces. Yet, the complex composition of biofilms often makes it challenging to characterize the individual signals and regulatory mechanisms. Developing tractable model systems to characterize these ancient co-evolved interactions is the key to understand fundamental processes in evolutionary biology. Here, we characterized for the first time two types of bacterial signaling molecules that induce the morphogenic transition and analyzed their abundance and combinatorial activity. This study highlights the crucial role of the converging activity of multiple bacterial signals in development-related cross-kingdom signaling.