Metatranscriptomic response of deep ocean microbial populations to infusions of oil and/or synthetic chemical dispersant.

Oil spills are a frequent perturbation to the marine environment that has rapid and significant impacts on the local microbiome. Previous studies have shown that exposure to synthetic dispersant alone did not enhance heterotrophic microbial activity or oxidation rates of specific hydrocarbon components but increased the abundance of some taxa (e.g., Colwellia). In contrast, exposure to oil, but not dispersants, increased the abundance of other taxa (e.g., Marinobacter) and stimulated hydrocarbon oxidation rates. Here, we advance these findings by interpreting metatranscriptomic data from this experiment to explore how and why specific components of the microbial community responded to distinct organic carbon exposure regimes. Dispersant alone was selected for a unique community and for dominant organisms that reflected treatment- and time-dependent responses. Dispersant amendment also led to diverging functional profiles among the different treatments. Similarly, oil alone was selected for a community that was distinct from treatments amended with dispersants. The presence of oil and dispersants with added nutrients led to substantial differences in microbial responses, likely suggesting increased fitness driven by the presence of additional inorganic nutrients. The oil-only additions led to a marked increase in the expression of phages, prophages, transposable elements, and plasmids (PPTEPs), suggesting that aspects of microbial community response to oil are driven by the "mobilome," potentially through viral-associated regulation of metabolic pathways in ciliates and flagellates that would otherwise throttle the microbial community through grazing.IMPORTANCEMicrocosm experiments simulated the April 2010 Deepwater Horizon oil spill by applying oil and synthetic dispersants (Corexit EC9500A and EC9527A) to deep ocean water samples. The exposure regime revealed severe negative alterations in the treatments' heterotrophic microbial activity and hydrocarbon oxidation rates. We expanded these findings by exploring metatranscriptomic signatures of the microbial communities during the chemical amendments in the microcosm experiments. Here we report how dominant organisms were uniquely associated with treatment- and time-dependent trajectories during the exposure regimes; nutrient availability was a significant factor in driving changes in metatranscriptomic responses. Remarkable signals associated with PPTEPs showed the potential role of mobilome and viral-associated survival responses. These insights underscore the time-dependent environmental perturbations of fragile marine environments under oil and anthropogenic stress.

Dispersant addition, but not nutrients, stimulated blooms of multiple hydrocarbonoclastic genera in nutrient-replete coastal marine surface waters.

The range of impacts of chemical dispersants on indigenous marine microbial communities and their activity remains poorly constrained. We tested the response of nearshore surface waters chronically exposed to oil leakage from a downed platform and supplied with nutrients by the Mississippi River to Corexit dispersant and nutrient additions. As assessed using 14C-labeled tracers, hexadecane mineralization potential was orders of magnitude higher in all unamended samples than in previously assessed bathypelagic communities. Nutrient additions stimulated microbial mortality but did not affect community composition and had no generalizable effect on hydrocarbon mineralization potential. By contrast, Corexit amendments caused a rapid shift in community composition and a drawdown of inorganic nitrogen and orthophosphate though no generalizable effect on hydrocarbon mineralization potential. The hydrocarbonoclastic community's response to dispersants is largely driven by the relative availability of organic substrates and nutrients, underscoring the role of environmental conditions and multiple interacting stressors on hydrocarbon degradation potential.