Metagenomic mining reveals extensive novelty, enhanced biodegradation potential, and untapped biosynthetic capacity...

Oil reservoir microorganisms represent a vast and largely unexplored reservoir of biological diversity and functional potential, yet comprehensive studies on their genomic and metabolic characteristics remain limited. To address this gap, we collected 101 metagenomic sequencing samples from 13 distinct oilfields across China. Through extensive de novo assembly and binning processes, we successfully reconstructed 3,057 medium and high-quality metagenome-assembled genomes (MAGs), providing an unprecedented genomic resource for reservoir microbiome research. Strikingly, 73.77% of these MAGs correspond to novel taxa at the species level, highlighting the significant unexplored microbial diversity in these environments. Detailed genomic analysis revealed that MAGs classified under the class Planctomycetia exhibited notably larger genome sizes, primarily driven by the expansion of specific gene families, suggesting adaptive evolutionary strategies in hydrocarbon-rich environments. Furthermore, we identified 68 genes implicated in anaerobic alkane biodegradation pathways, with samples from the Shengli oilfield demonstrating particularly enhanced biodegradation potential, indicating site-specific functional adaptations. Beyond biodegradation, our study uncovered three MAGs assigned to the genus Tistrella, which harbored a remarkable abundance of biosynthetic gene clusters (BGCs) for secondary metabolites. Additionally, 14 candidate antimicrobial peptides (cAMPs) were detected, signifying the potential for novel bioactive compound discovery. Critically, both the Tistrella MAGs and cAMPs were identified for the first time within petroleum reservoir ecosystems, underscoring the unique biotechnological value of these environments. This research not only expands our understanding of oil reservoir microbial communities but also emphasizes their substantial implications for industrial applications, including bioremediation, antimicrobial development, and sustainable resource management.IMPORTANCEThis study provides a groundbreaking genomic exploration of oil reservoir microbiomes across 13 Chinese oilfields, reconstructing 3,057 medium and high-quality metagenome-assembled genomes (MAGs). Remarkably, 73.77% of these MAGs represent novel species, revealing vast unexplored microbial diversity. We observed genome expansion in Planctomycetia lineages and identified 68 genes involved in anaerobic alkane degradation, with heightened biodegradation potential in Shengli oilfield samples. Crucially, we discovered three Tistrella MAGs rich in biosynthetic gene clusters (BGCs) for secondary metabolites and 14 candidate antimicrobial peptides (cAMPs), both reported for the first time in petroleum reservoirs. These findings highlight the immense biotechnological potential of reservoir microbiomes, offering new pathways for bioremediation strategies in oil-contaminated environments and novel sources for antimicrobial discovery. This work underscores the critical need for continued investigation into these unique ecosystems to harness their functional capabilities for energy sustainability and pharmaceutical innovation.