Environmental filtering drives cryptic diversity and shifting interaction networks across lake, ephemeral pond, and desiccated microbial mat communities in the Untersee Oasis, East Antarctica

Abstract Antarctic lakes and surrounding habitats are natural laboratories for studying microbial ecology in extreme environments, yet assembly and dispersal across these systems remain poorly understood. We analyzed bacterial (16S rRNA) and eukaryotic (18S rRNA) communities across benthic lake mats, pond mats, and desiccated mats around Lake Untersee, East Antarctica. Both domains showed significant environmental differentiation with stochastic assembly dominating, but eukaryotes exhibited stronger habitat-specific structuring. Core microbiomes revealed contrasting strategies: bacteria showed broad colonization with few dominant taxa, while eukaryotes maintained smaller cores anchored by Adineta vaga. Cyanobacterial indicators demonstrated complete strain-level turnover despite uniform phylum dominance. Dispersal patterns diverged strongly: prokaryotes exhibited substantial cross-habitat exchange (28-61%) while eukaryotes showed minimal dispersal (2-16%). Distance-decay relationships revealed significant spatial structuring (bacterial r=0.316-0.70; eukaryotic r=0.43-0.84). Cross-domain networks shifted from facilitative in ponds (65% positive) to competitive under desiccation (54% negative), suggesting resource limitation overrides facilitation at extremes. Functional predictions highlighted habitat specialization: lakes enriched in biogeochemical cycling, desiccated mats in stress tolerance, ponds in CRISPR genes. These findings reveal divergent strategies shaped by environmental filtering, dispersal limitation, and viral interactions, with implications for ecosystem connectivity and resilience. Importance Antarctic lake ecosystems serve as natural laboratories for understanding microbial community assembly under extreme conditions, yet connectivity between aquatic and terrestrial habitats remains poorly characterized. This study reveals fundamentally divergent ecological strategies between bacterial and eukaryotic communities across Lake Untersee’s contrasting environments. While bacteria maintain broad dispersal networks (28-61% cross-habitat exchange) with strain-level habitat specialization, eukaryotes exhibit strong dispersal limitation (2-16% exchange) despite occupying adjacent habitats. Most strikingly, cross-domain interaction networks shift from predominantly facilitative in ephemeral ponds (65% positive associations) to competitive under desiccation stress (54% negative associations), directly challenging the stress gradient hypothesis that predicts cooperation dominates in extreme environments. Combined with habitat-specific functional specialization—from biogeochemical cycling in lakes to stress tolerance in desiccated mats—these findings provide a mechanistic framework for predicting ecosystem connectivity, resilience, and responses to climate-driven habitat transitions in polar regions.