Ecological plasticity of Halanaerobium microorganisms across terrestrial saline to hypersaline subsurface environments

Members of the genus Halanaerobium are widely distributed in hypersaline environments, including oil and gas reservoirs, and saline lake sediment. However, a comprehensive understanding of their physiological traits, metabolic capacities, adaptive strategies, and biogeography remains limited. In this study, a strictly anaerobic and halophilic strain, H. saccharolyticum_B KY39 was isolated from produced water in the Zhongyuan Oilfield, China. Strain KY39 grew at 20-45°C, 2-30% salinity, pH 5.3-9.0, and up to 50 MPa hydrostatic pressure. It could ferment various Carbohydrates (e.g., glucose, xylose, sucrose, and maltose) or use mannitol and pyruvate as electron donors under Fe(III)-reducing conditions. Comparative genomic analyses of 31 high-quality Halanaerobium strains revealed an open pangenome. Genes involved in osmotic and pressure stress responses, including those related to osmoprotectant biosynthesis and ion transport, were highly conserved. The thiosulfate sulfurtransferase (TST) gene, responsible for converting thiosulfate to sulfite, was universally present. Notably, compared to the strains from saline lakes, those from oil and gas reservoirs possessed larger genomes and harbored a broader repertoire of genes related to peptidoglycan biosynthesis, nitrogen fixation, sulfur metabolism, biofilm formation, and carbohydrate uptake, suggesting enhanced metabolic flexibility and environmental adaptation. Moreover, a survey of the available metagenomes revealed that Halanaerobium species were globally distributed across diverse environments exhibiting a broader salinity range. In addition to oil and gas reservoirs and saline lakes, they also widely reside in soils, fermented foods, and marine ecosystems. Collectively, these findings advance the systematic understanding of ecological plasticity and metabolic versatility of Halanaerobium, shedding light on their ecological roles and potential industrial impacts.

Importance: Members of the genus Halanaerobium are prominent inhabitants of surface and deep subsurface hypersaline environments, yet their ecological roles and adaptive strategies remain poorly understood. Here, through the isolation of a novel strain from the production fluid of an oil field combined with comparative genomic analyses across the genus, we revealed the metabolic versatility, stress tolerance, and global distribution of Halanaerobium. Our findings underscore the ecological plasticity, functional diversity, and niche differentiation within this genus, providing fundamental insights into its potential industrial and environmental applications.