Algal Growth and Morphogenesis-Promoting Factors Released by Cold-Adapted Bacteria Contribute to the Resilience and Morphogenesis of the Seaweed Ulva (Chlorophyta) in Antarctica (Potter Cove)

Abstract Macroalgae are found in a variety of marine vegetation ecosystems around the world, contributing significantly to global net primary production. In particular, the sea lettuce species, i.e., members of the genus Ulva (Chlorophyta), are located in many ecological niches and are characterized by excellent adaptability to environmental changes but depend on essential associated bacteria, which release algal growth and morphogenesis-promoting-factors (AGMPFs). Our work investigated the hypothesis that bacteria need to be stress-adapted to provide sufficient amounts of AGMPFs for the growth and morphogenesis of Ulva throughout its life cycle, even under severe environmental conditions. Our study thus aimed to understand which bacteria contribute to overcoming a variety of stressors in polar regions. Green macroalgae were collected from Potter Cove, King George Island (Isla 25 de Mayo), Antarctica, to study the associated microbiome and, subsequently, to identify AGMPFs releasing bacteria. Therefore, microbiome analysis was combined with morphogenetic bioassays and chemical analysis, identifying bacteria essential for algal growth under Antarctic conditions. Hereby, axenic cultures of Ulva compressa (cultivar Ulva mutabilis , Ria Formosa, Portugal), previously developed as a model system for bacteria-induced algal growth and morphogenesis, were inoculated with freshly isolated and cultivable Antarctic bacteria to determine their morphogenetic activity. The exploratory microbiome investigation identified numerous cold-adapted AGMPF-producing bacteria. Unlike the temperate-adapted bacterial strains originally isolated from the U. mutabilis holobiont, the cold-adapted isolates Maribacter sp. BPC-D8 and Sulfitobacter sp. BPC-C4 released sufficient amounts of AGMPFs, such as thallusin and still unknown compounds, necessary for the morphogenesis of the Antarctic Ulva even at 2 °C. Our results illustrate the role of chemical mediators provided by bacteria in cross-kingdom interactions under cold conditions within aquatic systems. The newly isolated bacteria will enable further functional studies to understand the resilience of the holobiont Ulva and might be applied in algal aquaculture even under adverse conditions. The study highlights the importance of eco-physiological assays in microbiome analysis.