Metagenomic characterization reveals complex association of soil hydrocarbon-degrading bacteria

Culture-independent metagenomic analysis was used to characterize the population changes undergone by a soil bacterial community after exposure to hydrocarbon fuel. Upon exposure, the soil community changed from a diverse community dominated by unclassified bacteria to a more homogeneous population of hydrocarbon-degrading bacteria dominated by Achromobacter, Azospirillum and Pseudomonas species. Attempts to culture bacteria only led to the isolation of Pseudomonas and Achromobacter species, demonstrating the insufficiency of culturing methods to characterize microbiomes. Achromobacter was the most abundant genera in the fuel enrichments but these isolates were unable to grow in fuel as a monoculture. However, when co-cultured with other hydrocarbon-degrading bacteria, including the Pseudomonas isolates, Achromobacter grew to high cell densities. Genome sequencing identified the isolate with the lowest capacity for growth in fuel as Achromobacter spanius S6 and revealed this bacterium contains many genes required for degradation of aromatics. Further analysis demonstrated A. spanius S6 required biosurfactants from other bacteria in the consortia to access and metabolize hydrocarbons. The ability of A. spanius to degrade aromatics was demonstrated by GC-MS. This study demonstrates the effect of fuel on microbial communities and characterizes an important cooperative relationship in the hydrocarbon-degrading consortia of significant implications for biodegradation and bioremediation. •Metagenomics elucidate the impact of hydrocarbon fuel on the soil microbiome.•Fuel reduces microbial diversity and selects for hydrocarbon-degraders.•Achromobacter spanius is the most abundant species in fuel enrichments.•A cooperative relationship between A. spanius and other hydrocarbon-degraders.•A. spanius degrades aromatics employing biosurfactants from other bacterial species.