Integrated holobiont responses of the Antarctic brown seaweed Adenocystis utricularis to thermal stress under a climate change scenario.

The Antarctic intertidal zone hosts ecologically pivotal holobionts such as the brown macroalga Adenocystis utricularis, whose response to climate-driven stressors remains poorly understood. Here, we applied an integrative holobiont framework combining microbial community profiling, host physiological assays, and phycosphere metabolomics to assess how thermal stress (2°C vs. 8°C) influences microbiome dynamics, host stress responses, and algal surface chemistry after 5 days under experimental conditions. Results showed that warming induced a transient reduction in microbial diversity, with Shannon diversity decreasing at Day 3 under 8°C and returning to levels comparable to the control by Day 5, accompanied by marked community structural reorganization. Elevated temperature enriched Campylobacteria and Gammaproteobacteria, while Bacteroidia and Verrucomicrobia decreased. Functional predictions revealed a shift from nutrient cycling and carbon turnover at 2°C toward heterotrophy, fermentation, and bacterivory-related pathways at 8°C. Microbiome disruption was associated with impaired photosynthetic performance, increased oxidative damage, reduced antioxidant defenses, and altered osmolyte accumulation, under warming conditions. Untargeted metabolomics uncovered pronounced thermal reprogramming of the algal surface metabolome, with >98% of detected features remaining chemically uncharacterized. Detected key metabolites included ceramides, N-acyl amino acids, and amphipathic compounds with putative cytotoxic or antioxidant activities, many of which increased under 8°C. Together, these findings demonstrate that A. utricularis response to thermal stress emerges from dynamic host-microbiome-metabolome interactions. By linking microbial restructuring, host physiology, and metabolomic plasticity, our study highlights the holobiont as the operative unit of adaptation in Antarctic coastal ecosystems facing climate change.