Comparative Genomics Reveals Evidence of the Genome Reduction and Metabolic Potentials of Isolated from Challenger Deep Sediment of the Mariana Trench.

Hadal zones account for the deepest 45% of oceanic depth range and play an important role in ocean biogeochemical cycles. As the least-explored aquatic habitat on earth, further investigation is still required to fully elucidate the microbial taxonomy, ecological significance, metabolic diversity, and adaptation in hadal environments. In this study, a novel strain Lsc_1132 was isolated from sediment of the Mariana Trench at 10,954 m in depth. Strain Lsc_1132 contains heterogenous 16S rRNA genes, exhibiting the highest sequence similarities to the type strains of LMG 21831, , NBRC 102427, , and NBRC 102451, with a range of 98.60-99.10% identity. The highest average nucleotide identity (ANI), the highest digital DNA-DNA hybridization (DDH) values, and the average amino acid identity (AAI) with sp. PS3-40 reached 73.5%, 21.4%, and 75.54%, respectively. The major cellular fatty acids of strain Lsc_1132 included iso-C, Summed Feature 3 (C6c and/or Cc), iso-C, anteiso-C, and iso-C5c. The respiratory quinone of strains Lsc_1132 was MK-7. The G + C content of the genomic DNA was 40.9%. Based on the GTDB taxonomy and phenotypic data, strain Lsc_1132 could represent a novel species of a novel genus, proposed as gen. nov. sp. nov. (type strain Lsc_1132 = MCCC 1K09620). Metabolically, strain Lsc_1132 demonstrates a robust carbohydrate metabolism with many strain-specific sugar transporters. It also has a remarkable capacity for metabolizing amino acids and carboxylic acids. Genomic analysis reveals a streamlined genome in the organism, characterized by a significant loss of orthologous genes, including those involved in cytochrome c synthesis, aromatic compound degradation, and polyhydroxybutyrate (PHB) synthesis, which suggests its adaptation to low oxygen levels and oligotrophic conditions through alternative metabolic pathways. In addition, the reduced number of paralogous genes in strain Lsc_1132, together with its high protein-coding gene density, may further contribute to streamlining its genome and enhancing its genomic efficiency. This research expands our knowledge of hadal microorganisms and their metabolic strategies for surviving in extreme deep-sea environments.