The biological effects and expected fate of the vast amount of oil in the Gulf of Mexico from the Deepwater Horizon blowout are unknown owing to the depth and magnitude of this event. Hydrocarbon-degrading genes coincided with the concentration of various oil contaminants. Changes in hydrocarbon composition with distance from the source and incubation experiments with environmental isolates demonstrated faster-than-expected hydrocarbon biodegradation rates at 5 C. Based on these results, the potential exists for intrinsic bioremediation of the oil plume Hazen, T.
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Predicting the long-term fate of this oil is hindered by a lack of data about the combined influences of pressure, temperature, and sediment composition on microbial hydrocarbon remineralization in deep-sea sediments.
To investigate crude oil biodegradation by native GOM microbial communities, we incubated core-top sediments from 13 GOM sites at water depths from 60— m with crude oil under simulated aerobic seafloor conditions. Biodegradation occurred in all samples and followed a predictable compound class sequence dictated by molecular weight and structure.
Our results indicated a modest inhibitory effect of pressure on biodegradation over our experimental range. However, the expansion of oil exploration to deeper waters e. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. These subsurface oil plumes, rather than oil that reached surface waters, were considered a major source of oil to the seafloor, based on evidence of minimal photodegradation in oiled sediment samples [ 2 ].
Sinking high-density oil residues [ 6 ] and diffusion through the water column [ 7 ] may also have contributed to oil sedimentation. Little information about the fate of oil spilled in deep-sea environments was available before the Deepwater Horizon blowout, and it was unclear how much could be extrapolated from studies of previous spills in very different environments e. Exxon Valdez [ 8 ] and Gulf War [ 9 ]. Biodegradation is expected to be the major depletion mechanism of oil in deep, dark waters [ 10 ], where other common weathering processes in surface waters such as photooxidation and evaporation are not active.
This expectation was reinforced by studies that revealed the enrichment of indigenous oil-degrading microbes and upregulation of hydrocarbon-degrading genes in deep waters following the spill [ 11 — 14 ]. Deep sea environments, characterized by low temperature and high hydrostatic pressure, present energetic challenges to microbial metabolism. Among interconnected factors e. Laboratory incubation experiments [ 19 — 25 ] have demonstrated that some bacteria are capable of hydrocarbon degradation under elevated pressure, but the effect of pressure in these studies has been mixed.
Schwarz et al. Grossi et al. The expansion of oil exploration and production to deeper marine environments increases the likelihood of deep-sea oil spills.
However, laboratory studies of the effect of pressure on hydrocarbon biodegradation have only focused on the fate of individual oil model compounds e. Biodegradation occurring in the water column, however, might not represent that in sediments, owing to potential differences between the two systems such as microbial concentration and access to hydrocarbon substrates. In this work, we investigated the rate and extent of crude oil biodegradation in sediments from the Northern GOM, collected at water depths from 62— m, with a specific focus on the role of pressure.
We approximated in-situ temperatures and pressures of sediments in day incubation experiments with crude oil and examined changes in gas chromatography GC —amenable hydrocarbons. This is the first comparative study of crude oil biodegradation by indigenous microbes in sediments under deep and shallow marine conditions, designed to assess the potential for natural attenuation of spilled oil in GOM sediments. Field area was not on any private land, no permissions were required for collecting sediment cores at these sites and this study did not involve endangered or protected species.
Approximately 0. Incubation conditions approximated in-situ physical environments of the sediments: pressure ranged from 0. For each sediment site, we incubated oil-amended sediment in duplicate, with a parallel control of un-amended sediment. Sediments were incubated at pressures ranging from 0. Incubation vials in ambient pressure experiments 0. In addition, to further explore the effects of pressure, three deep sediment samples were incubated both at high pressures 9.
Because core-top sediments were relatively well-oxygenated in situ Table 1 , all experiments were carried out under aerobic conditions. Incubation vials were stirred at rpm with magnets to keep oxygen, sediments, and nutrients well-mixed over the course of the incubation period. Locations of 13 sampling sites across the Northern Gulf of Mexico at water depth ranging from 60—m. Circles are color-coded representing total organic content TOC, percent weight of sediments.
Schlitzer, R. CTD: conductivity-temperature-depth device, P: pressure, T: temperature. Incubation vials were centrifuged to separate aqueous and solid phases in order to measure the water fraction and sediment-associated oil components. Any visible oil on vial walls after decanting was recovered with additional sea water medium and transferred to the water fraction WAF. For each sample, both phases were extracted with an azeotrope of dichloromethane and methanol in a proportion of by volume three times.
N -alkane and branched alkanes were quantified using an alkane standard mix of C 7 -C 40 solution Sigma-Aldrich. To characterize and quantify biodegradation effects on oil components, we normalized compounds to internal biomarkers generally considered to be recalcitrant [ 29 — 31 ].
The relative loss of different compound classes was calculated as following t 0 and t f are the initial and final time points for the incubation : 1 2 We defined total n -alkanes as the sum of C 15—40 n -alkanes and total PAH as the sum of all PAHs analyzed S1 Table.
Compound loss patterns after incubation followed the canonical biodegradation sequence [ 31 — 34 ] and were consistent with field data on Macondo oil degradation [ 15 , 16 ]. The loss sequence was governed by molecular weights and structures; short chain alkanes were degraded to a greater extent than long chain alkanes S2 Fig , and straight chain n -alkanes were preferentially degraded over their saturated isoprenoid analogues Fig 2.
Long chain n -alkanes up to C 40 were degraded, suggesting that these long alkanes were more susceptible to biodegradation than C 30 hopane; these results contrast with those reported by Bagby et al. Total PAH decreased to a smaller extent than total n-alkanes, with the resistance to biodegradation increased with the number of rings and the degree of alkylation. For instance, 3-ring PAHs including phenanthrene and its alkylated homologues were depleted in most samples, whereas 4-ring PAHs such as pyrene and chrysene were only slightly degraded in the most degraded samples S3 Fig.
Compound groups such as hopanes, steranes, and TAS have been widely used as conservative tracers for oil, based on the assumption that they are relatively recalcitrant [ 29 — 31 ]. However, recent laboratory studies [ 35 — 37 ] and field data [ 15 , 16 ] have shown that these compounds can be more subject to biodegradation than previously thought.
We justified the treatment of C 30 hopane and C 26 TAS as conservative tracers in our study for two reasons. First, our incubation duration 18 days was shorter than the time scales of hopane and sterane biodegradation observed in the field [ 38 ] and experimentally.
After 18 days, total n -alkanes were depleted in all samples. Replicate incubations exhibited a small range of variability, with standard deviations from 0. Degradation of oil in both sediment and water fractions were relatively similar at each site.
For all samples incubated at higher pressures i. Error bars represent one standard deviations from the means. We also found inverse relationships between loss via biodegradation and water depth for other aliphatic compounds, including cyclohexanes, pristane, and phytane S4 and S5 Figs.
Sediments from the shallowest water depths incubated at 0. Samples incubated at 2. High pressure samples 9. This was surprising since the 15 MPa sample showed the least n-alkane depletion. This led us to consider the potential for an experimental artifact due to loss of volatile compounds during sample decompression following the incubation period. Biodegradation of hydrocarbons is often isomer-specific.
Isomers may share similar physicochemical properties yet be more or less susceptible to biodegradation [ 34 , 44 — 46 ], possibly due to enzyme specificity or steric considerations. At low pressures 2. In contrast, this ratio remained relatively constant in 15 MPa samples, indicating both compounds, which have similar vapor pressures, were loss during de-gassing to the same extent.
Thus, we concluded that biodegradation was indeed the major cause for n-alkane depletion at 15 MPa. The dashed arrow is interpreted as the direction of increasing biodegradation extent. Samples are color-coded according to sampling water depths.
Depletion in deep water samples are possibly due to off-gassing effect. Samples are color coded by pressures MPa. Even before anthropogenic influence, the GOM seafloor was subject to petroleum input via natural seeps average of , tons of petroleum annually [ 48 ], which have likely been active over millions of years.
Continued exposure may have primed GOM microbial communities to develop the capability to readily degrade hydrocarbons.
Prior exposure to hydrocarbons could accelerate biodegradation, as a memory response [ 49 ]. We speculated that our sediments were previously exposed to oil, based on the presence of background oil hydrocarbons including n -alkanes and C 30 hopane S4 Appendix.
This might explain the promptness in degrading oil of the GOM sediments seen in our study. The level of hydrocarbon contamination in sediments has been proposed to influence rates of biodegradation [ 16 , 51 , 52 ]. In our study, oil amendment led to an average concentration of 1. Samples at 2. There are inevitable challenges in isolating the effect of pressure on biodegradation. In previous studies of pressure effects, single inocula were incubated under both high and low pressure; either sea surface inocula were introduced to high pressure [ 26 ] or piezotolerant strains were placed in ambient pressure [ 19 , 20 ].
Introducing microbes to non-native conditions can impact their growth and carbon utilization [ 53 — 55 ]. In this study, we attempted to minimize this concern by comparing the hydrocarbon-degrading capacity of native sediment communities under approximated in-situ conditions although our sediments were exposed to surface conditions for a period after sampling. Given possible compromising factors deep-sea microbial communities encountered during sampling and experimental setup, we recognize that our results may provide a conservative estimation of biodegradation at high pressure.
To better understand the impact incubation under non-native conditions might have, we incubated three deep GOM sediments at both in situ seafloor 9. Hydrocarbon degradation in these high and low pressure treatments of the same sediments appeared to be stochastic. The DSH10 sample showed more extensive n-alkane biodegradation at surface pressure 0.
Conversely, the DSH08 sediment showed much less n-alkane degradation at surface pressure than at seafloor pressure 11 MPa. The PCB06 sample, however, showed virtually no difference in biodegradation between surface and seafloor pressure 9. The absence of a clear trend in this subset of our data may be the result of pressure-induced perturbation in sediment community. We conclude that, until technology for in-situ deep sea incubation [ 56 , 57 ] or pressure-retaining sampling [ 58 , 59 ] becomes more widely available, the best practice for hydrocarbon biodegradation studies is to incubate samples under conditions simulating their native, in-situ environments.
Our study assessed the rate and nature of oil biodegradation across the Northern GOM at a wide water depth range 60— m , representing a range of shallow water to approximately the depth of DWH spill. All sediments were found to degrade oil.
Piezotolerant microbial cultures at pressure up to 15 MPa demonstrated their capability to degrade oil, suggesting a high potential for natural attenuation of spilled oil.
Under optimal nutrients and oxygen availability, as provided here, we predict that it would take a minimum of 42 days for complete n-alkane degradation at 15 MPa, compared to average of 19 days at shallow sites 0. Our study focused on the early, oxic biodegradation of GC-amenable oil, after 18 days of incubation. Although pressure alone was not a major inhibitor of biodegradation in our experimental range, the expansion of oil exploration to deeper waters e.
Deep-sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria
Predicting the long-term fate of this oil is hindered by a lack of data about the combined influences of pressure, temperature, and sediment composition on microbial hydrocarbon remineralization in deep-sea sediments. To investigate crude oil biodegradation by native GOM microbial communities, we incubated core-top sediments from 13 GOM sites at water depths from 60— m with crude oil under simulated aerobic seafloor conditions. Biodegradation occurred in all samples and followed a predictable compound class sequence dictated by molecular weight and structure. Our results indicated a modest inhibitory effect of pressure on biodegradation over our experimental range. However, the expansion of oil exploration to deeper waters e. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Challenging Oil Bioremediation at Deep-Sea Hydrostatic Pressure
Deep-sea oil plume enriches psychrophilic oil-degrading bacteria
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