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The rate of crude oil biodegradation in the sea Roger C. Prince, Josh David Butler, and Aaron D. Redman Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b03207 • Publication Date (Web): 04 Oct 2016 Downloaded from http://pubs.acs.org on October 12, 2016
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initial 61 days
slick dispersed
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The rate of crude oil biodegradation in the sea
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Roger C. Prince*, Josh D. Butler and Aaron D. Redman
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ExxonMobil Biomedical Sciences, Inc.
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Annandale, NJ 08801
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*
[email protected] 9 10
Abstract
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Various groups have studied the rate of oil biodegradation in the sea over many years, but
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with no consensus on results. This can be attributed to many factors, but we show here
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that the principal confounding influence is the concentration of oil used in different
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experiments. Because of dilution, measured concentrations of dispersed oil in the sea are
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sub-ppm within a day of dispersal, and at such concentrations the rate of biodegradation
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of detectable oil hydrocarbons has an apparent half-life of 7-14 days. This can be
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contrasted with the rate of degradation at the higher concentrations found in oil slicks or
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when stranded on a shoreline; there the apparent half-life varies from many months to
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many years.
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Introduction
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Crude oil is used on an enormous scale – some 91 million barrels per day, 4.5 billion
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tonnes per year in 20131. Much of this is produced and/or transported in the marine
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environment, and despite the best efforts of industry and regulators, a small (and
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decreasing2) fraction gets spilled. Catastrophic accidents appropriately garner public and
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regulatory scrutiny. Oil spill response resources are available worldwide to respond and
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thereby minimize a spill’s environmental impact3. Providentially, crude oil has been part
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of the biosphere for millions of years, and even today natural seeps make up
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approximately half of the estimated 1.2 million tonnes of oil released to the world’s
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oceans every year4. This energy-rich resource feeds a diverse group of microorganisms5,6,
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and biodegradation is the eventual fate of at least the hydrocarbons of seep and spilled
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oil7.
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Catastrophic tanker spills usually make up only a few percent of the oil entering the sea
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every year4, although well blowouts8 and war releases9 can be larger. Nevertheless these
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point sources can result in substantial oil slicks that pose a serious threat to the
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environment. The preferred response is to collect the oil mechanically in booms and
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remove it with skimmers, but weather can overwhelm even the largest booming/skimmer
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efforts10. Responders then turn to dispersants to minimize the hazards of floating oil to
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birds, mammals and reptiles, and to reduce the amount of oil reaching shorelines11,12.
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Dispersants lower the interfacial tension between oil and water, allowing even minor
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turbulence to disperse oil as small droplets into the water column. An additional benefit is
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that this substantially increases the surface area of the spilled oil for microbial attack, and
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thus stimulates biodegradation13, and also gets the oil out of direct sunlight and its
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concomitant photooxidation14,15. Nevertheless, responders are appropriately concerned
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that the benefits of the dispersants must outweigh potential locally increased toxicity. A
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key question in this process is ‘How fast will oil be removed from the environment if it is
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dispersed?’, and much research has attempted to answer this question. Stewart et al.16
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reviewed early work, and there have been at least 22 papers on the topic since then (see
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Table S1). They present experiments under a range of conditions, and report half-lives for
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biodegradation that range from 1 to 276 days! (Table S1).
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Many factors likely affect the measured rates of oil biodegradation, including type of
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crude oil (although most work has focused on the hydrocarbon fraction, which to a first
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approximation is usually rather similar in different oils17), the microbial inoculum
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(adapted to hydrocarbons or not), the temperature, the mixing intensity, and potentially
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the nutrients (for example available nitrogen concentrations varied from natural seawater
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to >80mM, Table S1). But one factor often overlooked in explaining discrepancies in
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published work is the concentration of oil in the different experiments, which has varied
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over several orders of magnitude (2-10,000ppm, Table S1). As we will show below, the
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solubility of most hydrocarbons other than the small aromatics such as benzene, toluene,
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ethylbenzene and the xylenes is so low that the majority of hydrocarbons in most of the
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experiments cited above must have been in oil droplets, not in free solution.
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Biodegradation is thus probably a surface phenomenon, occurring at the oil-water
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interface, and therefore likely faster when this is maximized, for example when the oil
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droplets are very small. Indeed Brakstad et al.18 have shown that oil droplets of 10µm
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diameter degrade significantly faster than those of 30µm under identical conditions.
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We show here that the concentration of oil in a biodegradation experiment has a very
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significant effect on the apparent rate of biodegradation, and that the apparent half-life of
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both total hydrocarbon and individual species is proportional to concentration. Since
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measured concentrations of dispersed oil under successfully dispersed slicks or in
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submarine ‘plumes’ are very low (20 days for
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different hydrocarbons, and our data are reasonably consistent. We would expect
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different lag-times when enrichment cultures were used (Table S1).
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How does this information influence our understanding of the biodegradation of
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dispersed oil in the sea? First it is important to note that even our most dilute experiments
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are at concentrations above those measured in dispersed slicks and plumes19-23, so the
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fastest values reported here (Tables S4 and S5) should probably be regarded as
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conservative. Second, the rate of biodegradation of dispersed oil at low concentrations in
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unamended seawater is quite rapid – the half-life of (dilute total measurable)
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hydrocarbons is about 10 days. This can be compared to the half-life of the corralled slick
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of about 100 days (Figure 1), and contrasted with the rate of biodegradation of oil that
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gets to a shoreline, where the half-life can be of the order of years unless fertilizers are
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applied27. Third, even at 2.5 ppm oil, essentially all the alkanes and larger aromatics are
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not freely dissolved – they remain in oil droplets, albeit likely very small ones (62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62 >62
