Background Environmental variability shapes microbial community composition and function, yet its influence on microbial gene expression and host-microbiome interactions in sub-Antarctic regions remains poorly understood. Gills serve as the primary interface between aquatic organisms and their environment, harboring diverse and dynamic microbial communities that play a fundamental role in host physiology. Using a metatranscriptomic approach, this research aims to explore the influence of abiotic fluctuations in Patagonian fjords on the functional profile of the gill-associated microbiome in the southern king crab (Lithodes santolla) holobiont. By assessing shifts in microbial composition and gene expression, this research aims to uncover functional pathways linked to microbial metabolic adjustments and the host’s resilience. The findings provide insights into microbiome-driven functional responses in marine species and may inform conservation strategies under environmental change. Results Microbial gene expression profiles from individuals collected at two environmentally distinct locations, Ballena Sound and Choiseul Bay, revealed slight differences in microbial composition, with Proteobacteria dominating at both sites. Functional annotation identified key metabolic pathways involved in energy production, stress response, and microbial interactions, highlighting distinct adaptive mechanisms to environmental fluctuations. Differential expression analysis revealed shifts in carbon fixation, ion transport, and oxidative stress responses, suggesting that these physiological responses could be modeled by environmental conditions. Additionally, host-associated transcripts showed differential enrichment in immune regulation and metabolic homeostasis pathways, suggesting microbiome-mediated effects on host physiology. Conclusions These findings offer first insights into the dynamic relationship between environmental factors and microbial functionality in L. santolla, highlighting the significance of gill-associated microbiome plasticity in adapting to changing habitats. These results improve our understanding of microbiome-driven functional responses to sub-Antarctic environments, offering valuable perspectives for assessing holobiont resilience in these fluctuating ecosystems. Video Abstract
