Anaerobic degradation of hexadecane and phenanthrene coupled to sulfate reduction by enriched consortia from northern Gulf of Mexico seafloor sediment

Boryoung Shin,Will A Overholt,Karsten Zengler,Joel E Kostka,Kuk-Jeong Chin,Konstantinos T Konstantinidis,Lisa M Gieg,Minjae Kim

doi:10.1038/s41598-018-36567-x

Abstract

To advance understanding of the fate of hydrocarbons released from the Deepwater Horizon oil spill and deposited in marine sediments, this study characterized the microbial populations capable of anaerobic hydrocarbon degradation coupled with sulfate reduction in non-seep sediments of the northern Gulf of Mexico. Anaerobic, sediment-free enrichment cultures were obtained with either hexadecane or phenanthrene as sole carbon source and sulfate as a terminal electron acceptor. Phylogenetic analysis revealed that enriched microbial populations differed by hydrocarbon substrate, with abundant SSU rRNA gene amplicon sequences from hexadecane cultures showing high sequence identity (up to 98%) to Desulfatibacillum alkenivorans (family Desulfobacteraceae), while phenanthrene-enriched populations were most closely related to Desulfatiglans spp. (up to 95% sequence identity; family Desulfarculaceae). Assuming complete oxidation to CO2, observed stoichiometric ratios closely resembled the theoretical ratios of 12.25:1 for hexadecane and 8.25:1 for phenanthrene degradation coupled to sulfate reduction. Phenanthrene carboxylic acid was detected in the phenanthrene-degrading enrichment cultures, providing evidence to indicate carboxylation as an activation mechanism for phenanthrene degradation. Metagenome-assembled genomes (MAGs) revealed that phenanthrene degradation is likely mediated by novel genera or families of sulfate-reducing bacteria along with their fermentative syntrophic partners, and candidate genes linked to the degradation of aromatic hydrocarbons were detected for future study.

Highlights

In April 2010, the Deepwater Horizon (DWH) oil rig exploded and sank, discharging approximately 4.9 million barrels of crude oil into the Gulf of Mexico (GoM) at a depth of 1544 m over the course of 86 days[1,2]
Less information is available in comparison to aerobic biodegradation pathways, some evidence suggests that anaerobic hydrocarbon degradation was enhanced in Gulf of Mexico ecosystems impacted by oil from the DWH blowout
A number of strains have been isolated and their metabolic pathways characterized for anaerobic alkane degradation, whereas very little information is available on the biochemical mechanisms of anaerobic polycyclic aromatic hydrocarbons (PAHs) degradation

Summary

Introduction

In April 2010, the Deepwater Horizon (DWH) oil rig exploded and sank, discharging approximately 4.9 million barrels of crude oil into the Gulf of Mexico (GoM) at a depth of 1544 m over the course of 86 days[1,2]. Only one bacterial pure culture (Deltaproteobacterial strain NaphS2) has been obtained which is capable of anaerobic PAH degradation This strain belongs to the Desulfobacteraceae and was isolated from a naphthalene-degrading and sulfate-reducing enrichment culture from anoxic marine sediment[30]. Metabolic genes involved in both aerobic and anaerobic hydrocarbon degradation were enriched in deep-sea oil plumes generated from the spill[39]. The objectives of this study were (i) to characterize the microbial communities that mediate the mineralization of PHCs under sulfate-reducing conditions in anoxic sediments of the northern GoM seafloor, and (ii) to investigate the metabolic potential for anaerobic PAH degradation through a combination of metabolomics and metagenomics. We further provide the genomes of several novel organisms linked to respiratory and fermentative pathways during phenanthrene metabolism

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