The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments

Abstract

During hydrocarbon exposure, the composition and functional dynamics of marine microbial communities are altered, favoring bacteria that can utilize this rich carbon source. Initial exposure of high levels of hydrocarbons in aerobic surface sediments can enrich growth of heterotrophic microorganisms having hydrocarbon degradation capacity. As a result, there can be a localized reduction in oxygen potential within the surface layer of marine sediments causing anaerobic zones. We hypothesized that increasing exposure to elevated hydrocarbon concentrations would positively correlate with an increase in denitrification processes and the net accumulation of dinitrogen. This hypothesis was tested by comparing the relative abundance of genes associated with nitrogen metabolism and nitrogen cycling identified in 6 metagenomes from sediments contaminated by polyaromatic hydrocarbons from the Deepwater Horizon (DWH) oil spill in the Gulf of Mexico, and 3 metagenomes from sediments associated with natural oil seeps in the Santa Barbara Channel. An additional 8 metagenomes from uncontaminated sediments from the Gulf of Mexico were analyzed for comparison. We predicted relative changes in metabolite turnover as a function of the differential microbial gene abundances, which showed predicted accumulation of metabolites associated with denitrification processes, including anammox, in the contaminated samples compared to uncontaminated sediments, with the magnitude of this change being positively correlated to the hydrocarbon concentration and exposure duration. These data highlight the potential impact of hydrocarbon inputs on N cycling processes in marine sediments and provide information relevant for system scale models of nitrogen metabolism in affected ecosystems.

Keywords: deepwater horizon oil spill; denitrification; marine sediments; metagenomics; microbial ecology; nitrogen cycling; oil contamination; oil seeps.

Figure 1

Graphical representation of the changing relative abundance of different key nitrogen pathways and genes within each of the sample types.

Figure 2

Principal Components Analysis (PCA) of the relative abundance of nitrogen pathway gene annotation shared (33 genes) between the three samples types [oil spill (circles), oil seep (diamonds), and uncontaminated (triangles)]. Genes on the graph are given abbreviated names, but their full names and associated functional groups are given in Supplementary Table 2. The gene abundance loading values are given by the bottom and left axes. Samples from each group shown as shapes in gray with axes scores given by the top and right axes. Gene functions are colored by their level 2 annotation as specified at the right outer margin of the graph. The variance accounted for by each component is listed on each axis.