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Integrated Omics Elucidate the Mechanisms Driving the Rapid Biodegradation of Deepwater Horizon Oil in Intertidal Sediments Undergoing Oxic–Anoxic Cycles
journal contribution
posted on 2020-08-05, 19:43 authored by Smruthi Karthikeyan, Minjae Kim, Patrick Heritier-Robbins, Janet K. Hatt, Jim C. Spain, Will A. Overholt, Markus Huettel, Joel E. Kostka, Konstantinos T. KonstantinidisCrude oil buried in intertidal sands
may be exposed to alternating
oxic and anoxic conditions but the effect of this tidally induced
biogeochemical oscillation remains poorly understood, limiting the
effectiveness of remediation and managing efforts after oil spills.
Here, we used a combination of metatranscriptomics and genome-resolved
metagenomics to study microbial activities in oil-contaminated sediments
during oxic–anoxic cycles in laboratory chambers that closely
emulated in situ conditions. Approximately 5-fold higher reductions
in the total petroleum hydrocarbons were observed in the oxic as compared
to the anoxic phases with a relatively constant ratio between aerobic
and anaerobic oil decomposition rates even after prolonged anoxic
conditions. Metatranscriptomics analysis indicated that the oxic phases
promoted oil biodegradation in subsequent anoxic phases by microbially
mediated reoxidation of alternative electron acceptors like sulfide
and by providing degradation-limiting nitrogen through biological
nitrogen fixation. Most population genomes reconstructed from the
mesocosm samples represented uncultured taxa and were present typically
as members of the rare biosphere in metagenomic data from uncontaminated
field samples, implying that the intertidal communities are adapted
to changes in redox conditions. Collectively, these results have important
implications for enhancing oil spill remediation efforts in beach
sands and coastal sediments and underscore the role of uncultured
taxa in such efforts.