Riddles of Lost City: Chemotrophic Prokaryotes Drives Carbon, Sulfur, and Nitrogen Cycling at an Extinct Cold Seep, South China Sea

Deep-sea cold seeps are one of the most productive ecosystems that sustained by hydrocarbons carried by the fluid. Once the seep fluid ceases, the thriving autotrophic communities die out, terming as the extinct seep. But heterotrophic fauna can still survive even for thousands of years. The critical role of prokaryotes in active seeps are well defined, but their functions in extinct seeps are poorly understood to date. Here, we clarified the diversity, taxonomic specificity, interspecies correlation, and metabolic profiles of sediment prokaryotes at an extinct seep site of Haima cold seep, South China Sea. Alpha diversity of archaea significantly increased, while that of bacteria remained unchanged in extinct seep compared to active seep. However, archaea composition did not differ significantly at extinct seep from active or nonseep sites based on weighted-unifrac dissimilarity, while bacteria composition exhibited significant difference. Distribution of archaea and bacteria showed clear specificity to extinct seeps, indicating the unique life strategies here. Prokaryotes might live chemolithoautotrophically on cycling of inorganic carbon, sulfur, and nitrogen, or chemoorganotrophically on recycling of hydrocarbons. Notably, many of the extinct seep specific species and networked keystone lineages are classified as Proteobacteria. Regarding the functional diversity and metabolic flexibility of this clade, Proteobacteria is supposed to integrate the geochemical cycles and play a critical role in energy and resource supplement for microbiome in extinct seep. Collectively, our findings shed lights on the microbial ecology and functional diversity in extinct seeps, providing new understanding of biogeochemical cycling after fluid cessation. IMPORTANCE This research paper uncovered the potential mechanisms for microbiota mediated geochemical cycling in extinct cold seep, advancing our understanding in deep sea microbiology ecology.