Hydrocarbon degraders establish at the costs of microbial richness, abundance and keystone taxa after crude oil contamination in permafrost environments

Oil spills from pipeline ruptures are a major source of terrestrial petroleum pollution in cold regions. However, our knowledge of the bacterial response to crude oil contamination in cold regions remains to be further expanded, especially in terms of community shifts and potential development of hydrocarbon degraders. In this study we investigated changes of microbial diversity, population size and keystone taxa in permafrost soils at four different sites along the China-Russia crude oil pipeline prior to and after perturbation with crude oil. We found that crude oil caused a decrease of cell numbers together with a reduction of the species richness and shifts in the dominant phylotypes, while bacterial community diversity was highly site-specific after exposure to crude oil, reflecting different environmental conditions. Keystone taxa that strongly co-occurred were found to form networks based on trophic interactions, that is co-metabolism regarding degradation of hydrocarbons (in contaminated samples) or syntrophic carbon cycling (in uncontaminated samples). With this study we demonstrate that after severe crude oil contamination a rapid establishment of endemic hydrocarbon degrading communities takes place under favorable temperature conditions. Therefore, both endemism and trophic correlations of bacterial degraders need to be considered in order to develop effective cleanup strategies.