Colwellia and Marinobacter metapangenomes reveal species-specific responses to oil and dispersant exposure in deepsea microbial communities

Over 7 million liters of Corexit EC9500A and EC9527A were applied to the Gulf of Mexico in response to the Deepwater Horizon oil spill. The impacts of dispersants remain under debate and negative, positive, and inconclusive impacts have been reported. Here, metatrancriptomics was applied in the context of metapangenomes to microcosms that simulated environmental conditions comparable to the hydrocarbon-rich 1,100 m deep plume. Within this microcosm study, negative effects of dispersants on microbial hydrocarbon degradation were previously reported based on activity measurements and geochemical data. Transcriptional enrichment of Colwellia, a potential dispersant degrader, followed variable time-dependent trajectories due to interactions between oil, dispersants, and nutrients. The Colwellia metapangenome captured a mixture of environmental responses linked to the Colwellia psychrerythraea 34H genome and to the genomes of other members of the Colwellia genus. The activation of genes involved in lipid degradation, nitrogen metabolism, and membrane composition under oil or nutrient availability, suggested an opportunistic growth strategy for Colwellia. In contrast, transcripts of Marinobacter, a natural hydrocarbon degrader, increased only in oil treatments. Marinobacter transcripts largely recruited to the accessory metapangenome of Marinobacter sp. C18, the closest genomic reference. A complex response involving carbon and lipid metabolism, chemotaxis and a type IV secretion system suggested active energy-dependent processes in Marinobacter. These findings highlight chemistry-dependent responses in the metabolism of key hydrocarbon-degrading bacteria and underscore that dispersant-driven selection could temper the ability of the community to respond to hydrocarbon injection.