Abatus agassizii is an irregular sea urchin species which inhabits shallow waters of the Weddell sea in Antarctica. As a deposit-feeder, A. agassizii nutrition relies on the ingestion of the surrounding sediment in which it lives barely burrowed. Despite the low complexity of its feeding habit, it harbours a long and twice-looped digestive tract suggesting that it may host complex bacterial community. Here we characterized the gut microbiota of two A. agassizii populations at the south of the King George Island in the West Antarctic Peninsula. Using an amplicon sequencing approach targeting the 16S rRNA gene, the goals of this study were to explore the Abatus microbiota composition and functional capacity, evaluating its compartmentalization among the gut content and the gut membrane in comparison with the external sediment. Additionally, we aimed to define a core gut microbiota between A. agassizii populations to identify potential keystone bacteria taxa. Lastly, we examined the keystone taxa micro-diversity looking for compartment specialization pattern at the oligotype scale. Our results show that the diversity and the structure of the microbiota were mostly driven by the compartments, and in a lesser extent by the population site. Differential enrichments in specific bacterial taxa were observed in the gut content and the gut membrane. Predictive functional profiles revealed a marked compartmentalization of the microbiota with higher abundance in specific pathways as the sulfur cycle in the gut content and the amino acid metabolism. Further, the definition of a core microbiota allowed the identification of shared potential keystone taxa assigned to the Desulfobacula and Spirochaeta genera, and evidence of compartmentalization at a high taxonomic resolution (>97% sequence similarity of the 16S rRNA gene) has been observed. The ecological relevance of these keystone taxa is in the host metabolism is discussed.