Functional metagenomic and enrichment metatranscriptomic analysis of marine microbial activities within a marine oil spill area

Highlights: • Marine microbes around a drilling platform were surveyed under 12 culture conditions. • Metagenome revealed functional genes involved in degrading petroleum hydrocarbons. • Meta-transcriptome revealed expression patterns of petroleum-degradation genes. • Enrichment culture conditions of higher efficiency to degrade petroleum hydrocarbons were pointed out. Microorganisms can degrade petroleum hydrocarbons, providing the advantages of low cost and few side effects towards ecosystems. Here, we evaluated the mechanisms of microbial degradation of marine petroleum hydrocarbon using metagenomics and metatranscriptomics approaches in order to provide new insight into microbial degradation of petroleum hydrocarbon. Seawater samples were collected at a depth of ∼8 m from an area near a drilling platform in the Bohai Bay and metagenomic sequencing was used to evaluate the functional potential of these marine microbial communities. Metatranscriptomic sequencing, fluorescence in-situ hybridization experiments, and flow cytometry were also performed on the microbial communities of samples subjected to 12 different culture conditions. The data were also subjected to Weighted Gene Co-expression Network Analysis (WGCNA) and co-transcription data visualization to evaluate co-transcription of gene functions. Metagenomic sequencing indicated the presence of numerous genes that were related to petroleum hydrocarbon metabolism. Further, the high co-transcription of genes in multiple pathways, indicated that groups of genes were synergistically transcribed to metabolize petroleum hydrocarbons. Metatranscriptomics also showed that microbial metabolism was highly active in the enrichments and that the transcription of a large number of prokaryotic replication and repair genes were significantly up-regulated including those encoding for the type VI secretion system (T6SS) protein, DNA polymerase I, thymidine phosphorylase, mevalonate kinase, and two-component systems. Concomitantly, the transcription of ribosomal genes involved in translation and photosynthetic genes involved in energy metabolism were down-regulated. Overall, oil and oxygen presence can increase the oil-degradation rates and related genes' transcription. Lot different metabolisms are co-regulated to exploit nutrients derived from the metabolism of petroleum hydrocarbons. Our analysis of metagenomic, metatranscriptomic and degradation data in this study show that a widespread gene spectrum involved in oil-degradation and the cooperation among genes is of great importance.