Metabolite profiling reveals insights into the species-dependent cold stress response of the green seaweed holobiont Ulva (Chlorophyta)

The green seaweed Ulva (Chlorophyta) and its associated epibacterial microbiome form a functional holobiont that adapts to stress as a whole. As the macroalga provides carbon sources for bacteria and relies on algal growth and morphogenesis-promoting factors (AGMPF) released by bacteria, those cross-kingdom interactions are especially fascinating. We hypothesized that the Ulva holobionts from the warm-temperate Mediterranean-Atlantic and cold Antarctic habitats respond to cold stress differently depending on the production of highly polar low molecular weight compounds (LMWCs) with stress-regulating activity. We compared the microbiome of and metabolic changes in U. compressa (cultivar U. mutabilis), initially collected in Ria Formosa (Portugal), with that of U. bulbosa (strain AWI #1002) collected in Antarctica by performing a warm-cold temperature shift experiment. Microbiome analysis indicated significant differences between the two species and that the number of operational taxonomic units (OTUs) was lower in cultivated U. bulbosa than in freshly isolated Ulva; despite this, AGMPF-producing bacteria were detected in both holobionts. Significant differences in metabolite profiles were observed between both species using hydrophilic interaction liquid chromatography coupled with electrospray ionization mass spectrometry (HILIC-ESI-MS). Biomarkers such as dimethylsulfoniopropionate (DMSP) and taurine were identified following a temperature shift from 18 °C to 5 °C in the warm-temperate U. mutabilis and the cold-adapted U. bulbosa, respectively. Our findings show that metabolic changes in the holobiont in response to cold are species-dependent.