Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill

Microbial communities present in the Gulf of Mexico rapidly responded to the Deepwater Horizon oil spill. In deep water plumes, these communities were initially dominated by members of Oceanospirillales, Colwellia, and Cycloclasticus. None of these groups were abundant in surface oil slick samples, and Colwellia was much more abundant in oil-degrading enrichment cultures incubated at 4 °C than at room temperature, suggesting that the colder temperatures at plume depth favored the development of these communities. These groups decreased in abundance after the well was capped in July, but the addition of hydrocarbons in laboratory incubations of deep waters from the Gulf of Mexico stimulated Colwellia''s growth. Colwellia was the primary organism that incorporated ¹³C from ethane and propane in stable isotope probing experiments, and given its abundance in environmental samples at the time that ethane and propane oxidation rates were high, it is likely that Colwellia was active in ethane and propane oxidation in situ. Colwellia also incorporated ¹³C benzene, and Colwellia''s abundance in crude oil enrichments without natural gas suggests that it has the ability to consume a wide range of hydrocarbon compounds or their degradation products. However, the fact that ethane and propane alone were capable of stimulating the growth of Colwellia, and to a lesser extent, Oceanospirillales, suggests that high natural gas content of this spill may have provided an advantage to these organisms.     

Chemical data quantify Deepwater Horizon hydrocarbon flow rate and environmental distribution

Detailed airborne, surface, and subsurface chemical measurements, primarily obtained in May and June 2010, are used to quantify initial hydrocarbon compositions along different transport pathways (i.e., in deep subsurface plumes, in the initial surface slick, and in the atmosphere) during the Deepwater Horizon oil spill. Atmospheric measurements are consistent with a limited area of surfacing oil, with implications for leaked hydrocarbon mass transport and oil drop size distributions. The chemical data further suggest relatively little variation in leaking hydrocarbon composition over time. Although readily soluble hydrocarbons made up ∼25% of the leaking mixture by mass, subsurface chemical data show these compounds made up ∼69% of the deep plume mass; only ∼31% of the deep plume mass was initially transported in the form of trapped oil droplets. Mass flows along individual transport pathways are also derived from atmospheric and subsurface chemical data. Subsurface hydrocarbon composition, dissolved oxygen, and dispersant data are used to assess release of hydrocarbons from the leaking well. We use the chemical measurements to estimate that (7.8 ± 1.9) × 10⁶ kg of hydrocarbons leaked on June 10, 2010, directly accounting for roughly three-quarters of the total leaked mass on that day. The average environmental release rate of (10.1 ± 2.0) × 10⁶ kg/d derived using atmospheric and subsurface chemical data agrees within uncertainties with the official average leak rate of (10.2 ± 1.0) × 10⁶ kg/d derived using physical and optical methods.     

Scientific basis for safely shutting in the Macondo Well after the April 20, 2010 Deepwater Horizon blowout

As part of the government response to the Deepwater Horizon blowout, a Well Integrity Team evaluated the geologic hazards of shutting in the Macondo Well at the seafloor and determined the conditions under which it could safely be undertaken. Of particular concern was the possibility that, under the anticipated high shut-in pressures, oil could leak out of the well casing below the seafloor. Such a leak could lead to new geologic pathways for hydrocarbon release to the Gulf of Mexico. Evaluating this hazard required analyses of 2D and 3D seismic surveys, seafloor bathymetry, sediment properties, geophysical well logs, and drilling data to assess the geological, hydrological, and geomechanical conditions around the Macondo Well. After the well was successfully capped and shut in on July 15, 2010, a variety of monitoring activities were used to assess subsurface well integrity. These activities included acquisition of wellhead pressure data, marine multichannel seismic profiles, seafloor and water-column sonar surveys, and wellhead visual/acoustic monitoring. These data showed that the Macondo Well was not leaking after shut in, and therefore, it could remain safely shut until reservoir pressures were suppressed (killed) with heavy drilling mud and the well was sealed with cement.     

Review of flow rate estimates of the Deepwater Horizon oil spill

The unprecedented nature of the Deepwater Horizon oil spill required the application of research methods to estimate the rate at which oil was escaping from the well in the deep sea, its disposition after it entered the ocean, and total reservoir depletion. Here, we review what advances were made in scientific understanding of quantification of flow rates during deep sea oil well blowouts. We assess the degree to which a consensus was reached on the flow rate of the well by comparing in situ observations of the leaking well with a time-dependent flow rate model derived from pressure readings taken after the Macondo well was shut in for the well integrity test. Model simulations also proved valuable for predicting the effect of partial deployment of the blowout preventer rams on flow rate. Taken together, the scientific analyses support flow rates in the range of ∼50,000–70,000 barrels/d, perhaps modestly decreasing over the duration of the oil spill, for a total release of ∼5.0 million barrels of oil, not accounting for BP''s collection effort. By quantifying the amount of oil at different locations (wellhead, ocean surface, and atmosphere), we conclude that just over 2 million barrels of oil (after accounting for containment) and all of the released methane remained in the deep sea. By better understanding the fate of the hydrocarbons, the total discharge can be partitioned into separate components that pose threats to deep sea vs. coastal ecosystems, allowing responders in future events to scale their actions accordingly.     

From the Cover: Footprint of Deepwater Horizon blowout impact to deep-water coral communities

On April 20, 2010, the Deepwater Horizon (DWH) blowout occurred, releasing more oil than any accidental spill in history. Oil release continued for 87 d and much of the oil and gas remained in, or returned to, the deep sea. A coral community significantly impacted by the spill was discovered in late 2010 at 1,370 m depth. Here we describe the discovery of five previously unknown coral communities near the Macondo wellhead and show that at least two additional coral communities were impacted by the spill. Although the oil-containing flocullent material that was present on corals when the first impacted community was discovered was largely gone, a characteristic patchy covering of hydrozoans on dead portions of the skeleton allowed recognition of impacted colonies at the more recently discovered sites. One of these communities was 6 km south of the Macondo wellhead and over 90% of the corals present showed the characteristic signs of recent impact. The other community, 22 km southeast of the wellhead between 1,850 and 1,950 m depth, was more lightly impacted. However, the discovery of this site considerably extends the distance from Macondo and depth range of significant impact to benthic macrofaunal communities. We also show that most known deep-water coral communities in the Gulf of Mexico do not appear to have been acutely impacted by the spill, although two of the newly discovered communities near the wellhead apparently not impacted by the spill have been impacted by deep-sea fishing operations.The explosion of the Deepwater Horizon (DWH) drilling rig at the Macondo wellhead site created an oil spill with characteristics unlike those of previous major oil spills where the release occurred either on the ocean surface or at shallow depths (1, 2). Because of the physics of the release, as well as the extensive use of dispersants, much of the oil and gas remained at depth (3–6). In addition, weathering, burning, and application of dispersants to surface slicks resulted in a return of additional hydrocarbons to the deep sea (5, 7, 8). The potentially toxic hydrocarbons and dispersants had the potential to impact numerous deep-sea communities that are inherently difficult to assess. In October 2010, beginning 90 d after the wellhead was capped, we visited 13 deep-water coral sites spread over a depth range of 350–2,600 m and from 87.31° to 93.60° W in the Gulf of Mexico (GoM), and did not detect visual indications of acute effects to coral communities at any of these sites. However, on November 2, 2010, we discovered a previously unknown coral community 13 km away from the Macondo wellhead that had clearly suffered a recent severe adverse impact, and oil forensics indicated that hydrocarbons found on corals at the site originated from the Macondo wellhead (9, 10). Following that discovery, we made a systematic effort to discover additional communities in the vicinity of the wellhead and then determine the status of the corals in these communities.Locating deep-water coral communities in the GoM is a laborious process as these communities are rare, relatively small, and there is no known remote-sensing method to unambiguously locate them. Most corals require a stable, hard substrate upon which to settle and grow (11). However, most of the sea floor in the deep GoM is soft sediment. The primary exception in the deep northern Gulf are authigenic carbonates which are formed as an indirect byproduct of anaerobic hydrocarbon degradation by bacteria in areas with hydocarbon seepage (12, 13). Authigenic carbonates form hardgrounds that are often suitable for a variety of attached megafauna and associated biological communities, including in some cases, corals (14).     

Chemical dispersants can suppress the activity of natural oil-degrading microorganisms

During the Deepwater Horizon oil well blowout in the Gulf of Mexico, the application of 7 million liters of chemical dispersants aimed to stimulate microbial crude oil degradation by increasing the bioavailability of oil compounds. However, the effects of dispersants on oil biodegradation rates are debated. In laboratory experiments, we simulated environmental conditions comparable to the hydrocarbon-rich, 1,100 m deep plume that formed during the Deepwater Horizon discharge. The presence of dispersant significantly altered the microbial community composition through selection for potential dispersant-degrading Colwellia, which also bloomed in situ in Gulf deep waters during the discharge. In contrast, oil addition to deepwater samples in the absence of dispersant stimulated growth of natural hydrocarbon-degrading Marinobacter. In these deepwater microcosm experiments, dispersants did not enhance heterotrophic microbial activity or hydrocarbon oxidation rates. An experiment with surface seawater from an anthropogenically derived oil slick corroborated the deepwater microcosm results as inhibition of hydrocarbon turnover was observed in the presence of dispersants, suggesting that the microcosm findings are broadly applicable across marine habitats. Extrapolating this comprehensive dataset to real world scenarios questions whether dispersants stimulate microbial oil degradation in deep ocean waters and instead highlights that dispersants can exert a negative effect on microbial hydrocarbon degradation rates.Crude oil enters marine environments through geophysical processes at natural hydrocarbon seeps (1) at a global rate of ∼700 million liters per year (2). In areas of natural hydrocarbon seepage, such as the Gulf of Mexico (hereafter, the Gulf), exposure of indigenous microbial communities to oil and gas fluxes can select for microbial populations that use petroleum-derived hydrocarbons as carbon and energy sources (3, 4). The uncontrolled deep-water oil well blowout that followed the explosion and sinking of the Deepwater Horizon (DWH) drilling rig in 2010 released about 750 million liters of oil into the Gulf. Seven million liters of chemical dispersants were applied (5) with the goal of dispersing hydrocarbons and stimulating oil biodegradation. A deep-water (1,000–1,300 m) plume, enriched in hydrocarbons (6–11) and dioctyl sodium sulfosuccinate (DOSS) (12, 13), a major component of chemical dispersants (14), formed early in the discharge (7). The chemistry of the hydrocarbon plume significantly altered the microbial community (11, 15–17), driving rapid enrichment of low-abundance bacterial taxa such as Oceanospirillum, Cycloclasticus, and Colwellia (18). The natural hydrocarbon degraders in Gulf waters were either in low abundance or absent in DWH deep-water plume samples (18).Chemical dispersants emulsify surface oil slicks, reduce oil delivery to shorelines (19), and increase dissolved oil concentrations, which should make oil more bioavailable (20) and stimulate biodegradation (21). The efficacy of dispersants in stimulating oil biodegradation is debated (22) and negative environmental effects have been documented (23). Dispersant application often requires ecological tradeoffs (24). Surprisingly little is known about the impacts of dispersants on the activity and abundance of hydrocarbon-degrading microorganisms (25). This work addressed three key questions: (i) Do dispersants influence microbial community composition? (ii) Is the indigenous microbial community as effective at oil biodegradation as microbial populations following dispersant/dispersed oil exposure? (iii) Does chemically dispersed oil stimulate hydrocarbon biodegradation rates?Laboratory experiments were used to unravel the effects of oil-only (supplied as a water-accommodated fraction, “WAF”), Corexit 9500 (“dispersant-only”), oil–Corexit 9500 mixture (chemically enhanced water-accommodated fraction, CEWAF) or a CEWAF with nutrients (CEWAF + nutrients) (SI Appendix) on Gulf deep-water microbial populations (SI Appendix, SI Text and Figs. S1 and S2). Experimental conditions (SI Appendix, Table S1) mimicked those prevailing in the DWH deep-water hydrocarbon plume (6–13, 18), the chemistry of which varied substantially over space and time (18). Amending samples with WAFs and CEWAFs assured that observed differences in microbial community composition and activity would be driven by compositional differences (e.g., the presence or absence of dispersants) in the dissolved organic carbon (DOC) pool rather than by differences in the bulk DOC concentration (26, 27). We developed an improved radiotracer method to directly quantify hydrocarbon oxidation rates. The microbial community composition was monitored over time using 16S rRNA amplicon sequencing. Dispersant application selected for specific microbial taxa and oligotypes with 16S rRNA gene sequences similar to those recovered in situ during the DWH discharge. Surprisingly, CEWAF (± nutrients) addition did not enhance microbial activity or microbial oil-degradation rates.     

Fallout plume of submerged oil from Deepwater Horizon

The sinking of the Deepwater Horizon in the Gulf of Mexico led to uncontrolled emission of oil to the ocean, with an official government estimate of ∼5.0 million barrels released. Among the pressing uncertainties surrounding this event is the fate of ∼2 million barrels of submerged oil thought to have been trapped in deep-ocean intrusion layers at depths of ∼1,000–1,300 m. Here we use chemical distributions of hydrocarbons in >3,000 sediment samples from 534 locations to describe a footprint of oil deposited on the deep-ocean floor. Using a recalcitrant biomarker of crude oil, 17α(H),21β(H)-hopane (hopane), we have identified a 3,200-km² region around the Macondo Well contaminated by ∼1.8 ± 1.0 × 10⁶ g of excess hopane. Based on spatial, chemical, oceanographic, and mass balance considerations, we calculate that this contamination represents 4–31% of the oil sequestered in the deep ocean. The pattern of contamination points to deep-ocean intrusion layers as the source and is most consistent with dual modes of deposition: a “bathtub ring” formed from an oil-rich layer of water impinging laterally upon the continental slope (at a depth of ∼900–1,300 m) and a higher-flux “fallout plume” where suspended oil particles sank to underlying sediment (at a depth of ∼1,300–1,700 m). We also suggest that a significant quantity of oil was deposited on the ocean floor outside this area but so far has evaded detection because of its heterogeneous spatial distribution.The sinking of the Deepwater Horizon in the Gulf of Mexico led to the discharge of ∼5.0 million barrels of petroleum from the Macondo Well. The discharge occurred at a water depth of ∼1,500 m and gave rise to intrusion layers (1) in the deep ocean that included both water-soluble hydrocarbons in the dissolved phase (2–6) and small particles of water-insoluble hydrocarbons (7–11). These intrusion layers were found primarily at a depth of 1,000–1,300 m and may have hosted the majority of the environmental discharge, including all the natural gas and ∼2 million barrels of liquid oil (12). Although the most abundant of the water-soluble hydrocarbons underwent rapid biodegradation during the spill (4, 6, 8, 9, 13–15), the fate and impacts of the insoluble hydrocarbons in the deep ocean have remained uncertain (16).The intrusion layers that hosted hydrocarbon contamination persisted for 6 mo or more and at distances >300 km from the well, but available evidence suggests that particles of submerged oil were particularly concentrated during the first 6 wk of discharge and within ∼15 km of the well (8, 9, 11). Thus, initial partitioning of hydrocarbon particles to the intrusion layers appears to have given way to transport or removal by undefined deep-ocean processes. Such processes might include sedimentation, buoyant rise toward the sea surface, incorporation into pelagic biota, biodegradation, or interventions at the wellhead. Mechanisms exist that support several of these options (9, 17–20), but uncertainty as to oil’s actual partitioning, the effect of chemical dispersant (21), and the impacts of a changing microbial community (6, 8, 9, 13–15, 17, 22–24) have precluded further understanding of the processes that acted on the oil.In this study we focus on testing the hypothesis that oil particles suspended in the deep intrusion layers were deposited on the sea floor over a broad area. To do so, we use publicly available data generated as part of the ongoing Natural Resource Damage Assessment (NRDA) process (Supporting Information) to assess the spatial distribution of petroleum hydrocarbons in the deep-ocean sediments of the Gulf of Mexico. We focus on the recalcitrant compound 17α(H),21β(H)-hopane (hereafter referred to as “hopane”) as a conserved tracer for crude oil deposition to sediments (25); we treat hopane as a degradation-resistant proxy for Macondo’s liquid-phase oil (26). Analysis of the spatial distribution of hopane allows us to define both a regional background level and a depositional footprint of oil from the Deepwater Horizon event. In combination with other lines of evidence, this analysis leads us to conclude that significant quantities of particulate oil sank from the intrusion layers to rest on the underlying sea floor.     

Genomic and physiological footprint of the Deepwater Horizon oil spill on resident marsh fishes

The biological consequences of the Deepwater Horizon oil spill are unknown, especially for resident organisms. Here, we report results from a field study tracking the effects of contaminating oil across space and time in resident killifish during the first 4 mo of the spill event. Remote sensing and analytical chemistry identified exposures, which were linked to effects in fish characterized by genome expression and associated gill immunohistochemistry, despite very low concentrations of hydrocarbons remaining in water and tissues. Divergence in genome expression coincides with contaminating oil and is consistent with genome responses that are predictive of exposure to hydrocarbon-like chemicals and indicative of physiological and reproductive impairment. Oil-contaminated waters are also associated with aberrant protein expression in gill tissues of larval and adult fish. These data suggest that heavily weathered crude oil from the spill imparts significant biological impacts in sensitive Louisiana marshes, some of which remain for over 2 mo following initial exposures.     

Air quality implications of the Deepwater Horizon oil spill

During the Deepwater Horizon (DWH) oil spill, a wide range of gas and aerosol species were measured from an aircraft around, downwind, and away from the DWH site. Additional hydrocarbon measurements were made from ships in the vicinity. Aerosol particles of respirable sizes were on occasions a significant air quality issue for populated areas along the Gulf Coast. Yields of organic aerosol particles and emission factors for other atmospheric pollutants were derived for the sources from the spill, recovery, and cleanup efforts. Evaporation and subsequent secondary chemistry produced organic particulate matter with a mass yield of 8 ± 4% of the oil mixture reaching the water surface. Approximately 4% by mass of oil burned on the surface was emitted as soot particles. These yields can be used to estimate the effects on air quality for similar events as well as for this spill at other times without these data. Whereas emission of soot from burning surface oil was large during the episodic burns, the mass flux of secondary organic aerosol to the atmosphere was substantially larger overall. We use a regional air quality model to show that some observed enhancements in organic aerosol concentration along the Gulf Coast were likely due to the DWH spill. In the presence of evaporating hydrocarbons from the oil, NO_x emissions from the recovery and cleanup operations produced ozone.On April 20, 2010, an explosion and subsequent leak beneath the Deepwater Horizon (DWH) drilling platform led to the largest marine oil spill in United States history. The air quality issues arising from the oil spill are different for workers at the site than for the population along the coast. Primary emissions are of more concern near the site and secondary pollutants are more important downwind. The key atmospheric pollutants considered in this paper are hydrocarbons (HCs), particulate matter (PM) or aerosol particles, ozone, carbon monoxide, and nitrogen oxides. Four sources of primary air pollutants attributable to the DWH oil spill are detected in our observations: (a) HCs evaporating from the oil; (b) smoke from deliberate burning of the oil slick; (c) combustion products from the flaring of recovered natural gas; and (d) ship emissions from the recovery and cleanup operations. Here, we examine these primary emissions and the subsequent production of ozone and secondary organic aerosol (SOA). Furthermore, we use aircraft data to derive the amount of atmospheric particulate matter formed per mass of oil that reached the surface. These results can be used to estimate implications for air quality during the DWH spill at other times and locations and can also provide information about effects on air quality by past or future spills.     

Federal seafood safety response to the Deepwater Horizon oil spill

Following the 2010 Deepwater Horizon oil spill, petroleum-related compounds and chemical dispersants were detected in the waters of the Gulf of Mexico. As a result, there was concern about the risk to human health through consumption of contaminated seafood in the region. Federal and Gulf Coast State agencies worked together on a sampling plan and analytical protocols to determine whether seafood was safe to eat and acceptable for sale in the marketplace. Sensory and chemical methods were used to measure polycyclic aromatic hydrocarbons (PAHs) and dispersant in >8,000 seafood specimens collected in federal waters of the Gulf. Overall, individual PAHs and the dispersant component dioctyl sodium sulfosuccinate were found in low concentrations or below the limits of quantitation. When detected, the concentrations were at least two orders of magnitude lower than the level of concern for human health risk. Once an area closed to fishing was free of visibly floating oil and all sensory and chemical results for the seafood species within an area met the criteria for reopening, that area was eligible to be reopened. On April 19, 2011 the area around the wellhead was the last area in federal waters to be reopened nearly 1 y after the spill began. However, as of November 9, 2011, some state waters off the Louisiana coast (Barataria Bay and the Delta region) remain closed to fishing.On April 22, 2010, 2 d after the explosion on the Deepwater Horizon (DWH) drilling platform, the rig collapsed and the wellhead failed. The explosion resulted in the loss of human life and the uncontrolled release of >200 million gallons of Louisiana light crude oil occurring ∼5,000 feet below the sea surface. DWH was declared a Spill of National Significance on April 29, 2010 and became the largest oil spill in US history (1). Among the significant human and environmental impacts of the spill, marine fisheries and supporting marine and estuarine ecosystems were subjected to contamination by crude oil, compromising the safety of seafood resources (1). An immediate and coordinated federal and state response ensued to safeguard seafood safety. Federal and state agencies mobilized personnel and resources to begin sampling seafood on April 28, 2010. Federal and state fishery closures were guided by observations of where oil was seen and forecasted to spread on the basis of climatic and hydrographic models (2). Seafood was collected around the periphery of the closed areas and from dockside and seafood market outlets across the Gulf coast and analyzed for oil-spill related contaminants to assess the effectiveness of the fishery closures. When the flow of oil was stopped on July 15, 2010 and the oil began to dissipate, sampling and analyses were conducted to determine whether seafood from previously closed areas was safe for harvest and human consumption. Sampling of reopened areas in federal waters continued through June 2011. We describe how federal agencies, working with the states, developed seafood safety criteria and protocols. In addition, sampling schemes, analyses, and data reporting for seafood safety efforts conducted in federal waters are provided. Results of testing the seafood collected in federal waters are also discussed.     

Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish

The Deepwater Horizon disaster released more than 636 million L of crude oil into the northern Gulf of Mexico. The spill oiled upper surface water spawning habitats for many commercially and ecologically important pelagic fish species. Consequently, the developing spawn (embryos and larvae) of tunas, swordfish, and other large predators were potentially exposed to crude oil-derived polycyclic aromatic hydrocarbons (PAHs). Fish embryos are generally very sensitive to PAH-induced cardiotoxicity, and adverse changes in heart physiology and morphology can cause both acute and delayed mortality. Cardiac function is particularly important for fast-swimming pelagic predators with high aerobic demand. Offspring for these species develop rapidly at relatively high temperatures, and their vulnerability to crude oil toxicity is unknown. We assessed the impacts of field-collected Deepwater Horizon (MC252) oil samples on embryos of three pelagic fish: bluefin tuna, yellowfin tuna, and an amberjack. We show that environmentally realistic exposures (1–15 µg/L total PAH) cause specific dose-dependent defects in cardiac function in all three species, with circulatory disruption culminating in pericardial edema and other secondary malformations. Each species displayed an irregular atrial arrhythmia following oil exposure, indicating a highly conserved response to oil toxicity. A considerable portion of Gulf water samples collected during the spill had PAH concentrations exceeding toxicity thresholds observed here, indicating the potential for losses of pelagic fish larvae. Vulnerability assessments in other ocean habitats, including the Arctic, should focus on the developing heart of resident fish species as an exceptionally sensitive and consistent indicator of crude oil impacts.The Deepwater Horizon disaster resulted in the release of more than 4 million barrels (636 million L) of oil into the offshore waters of the northern Gulf of Mexico between April 10 and July 14, 2010 (1). Although subsurface application of dispersant near the wellhead resulted in retention of a considerable portion of oil in the bathypelagic zone (2), oil also traveled to the upper surface waters where it formed a large and dynamic patchwork of slicks (e.g., covering an estimated 17,725 km² during May 2010) (3). In the decades following the last major US oil spill (the 1989 Exxon Valdez spill in Alaska), developing fish embryos have been shown to be especially vulnerable to the toxicity of crude oil (4). The northern Gulf provides critical spawning and rearing habitats for a range of commercially and ecologically important pelagic fish species, and the timing of oil release into the ecosystem from the damaged Deepwater Horizon/MC252 well coincided with the temporal spawning window for bluefin and yellowfin tunas, mahi mahi, king and Spanish mackerels, greater and lesser amberjack, sailfish, blue marlin, and cobia (5–13). Yellowfin tuna (Thunnus albacares) and greater amberjack (Seriola dumerili) contribute to important commercial fisheries (48,960,000 pounds in 2010 and 4,348,000 pounds in 2004, respectively) (14, 15). The Atlantic bluefin tuna (Thunnus thynnus) population from the Gulf of Mexico is currently at a historically low level (16), and was recently petitioned for listing under the US Endangered Species Act. For these and other pelagics, the extent of early-life stage loss from oiled spawning habitats is an important outstanding question for fisheries management and conservation.The developing fish heart is known as a sensitive target organ for the toxic effects of crude oil-derived polycyclic aromatic hydrocarbons (PAHs) (4). Of the multiple two- to six-ringed PAH families contained in crude oil, the most abundant three-ringed compounds are sufficient to drive the cardiotoxicity of petroleum-derived PAH mixtures. These compounds (fluorenes, dibenzothiophenes, and phenanthrenes) directly disrupt fish cardiac function (17, 18), thereby interfering with the interdependent processes of circulation and heart chamber formation. Exposure of fish embryos to PAH mixtures derived from crude oil slows the heartbeat (bradycardia) and reduces contractility (17, 19–21). The underlying mechanism was recently shown to be blockade of key potassium and calcium ion channels involved in cardiac excitation-contraction coupling (22). These collective effects of PAHs during embryonic and larval stages can influence the structure and function of the adult fish heart in ways that permanently reduce cardiac performance (23), potentially leading to delayed mortality. Consistent with this, mark-recapture studies on pink salmon following the Exxon Valdez spill found that transient and sublethal exposures to crude oil at very low levels during embryogenesis reduced subsequent marine survival to adulthood by 40% (24, 25). Exposures to relatively higher PAH concentrations cause embryonic heart failure and death soon after fish hatch into free-swimming larvae (19, 20, 23). These effects occur at a total PAH concentration range as low as 1–10 µg/L for more sensitive species (26, 27), levels as much as an order-of-magnitude lower than those measured in some samples collected both at depth and at the surface during the Deepwater Horizon active spill phase (28, 29).The above crude oil cardiotoxicity syndrome has been extensively characterized in zebrafish embryos exposed to several geologically distinct oils (17, 21, 23, 30, 31), including the Mississippi Canyon 252 (MC252) crude oil released from the blown out Deepwater Horizon wellhead (20, 32). Similar effects have been reported for temperate marine and anadromous species, such as Pacific herring (19, 26, 27, 33) and pink salmon (34, 35), following exposure to Alaska North Slope crude oil. Although zebrafish are a tropical freshwater model species, the embryos of herring and salmon assessed in the aftermath of the Exxon Valdez spill develop at cold temperatures (4–12 °C) over relatively long intervals (weeks to months). In contrast, pelagic species spawning in the warm surface waters of the northern Gulf of Mexico (e.g., 24–29 °C) develop rapidly (24–48 h to hatch) (36, 37). The influence of development duration on PAH uptake and toxicity, if any, is not well understood. The higher temperatures characteristic of waters in the Gulf of Mexico may also influence how the chemical composition of crude oil in surface habitat(s) changes over time (i.e., weathers). Processes that determine weathering are generally accelerated at higher temperatures, potentially influencing the fraction of cardiotoxic PAHs that is bioavailable for uptake by floating fish embryos in the mixed layer and thermocline regions. To address these information gaps, controlled laboratory exposures are necessary to determine the sensitivity of Gulf species to Deepwater Horizon crude oil.To assess potential early life-stage losses from large pelagic predator populations that were actively spawning in habitats affected by the Deepwater Horizon spill, we determined the effects of field-collected MC252 oil samples on the development of embryos from representative warm water open-ocean fish species. Our approach extended earlier work in zebrafish, a laboratory model species and Pacific herring, a marine nearshore spawner (19, 27, 38). Zebrafish and herring both produce large demersal embryos that are relatively easy to manipulate (i.e., collect, dechorionate, and image at consistent ontogenetic intervals). In contrast, Gulf pelagic species produce small, fragile, buoyant embryos that develop relatively rapidly (on a timescale of hours relative to days or weeks for zebrafish and herring, respectively) and are not amenable to dechorionation. Moreover, the embryos hatch into buoyant larvae. Normally present in infinite-volume pelagic habitats, they are very sensitive to any form of physical contact, thereby complicating conventional embryology in small-volume laboratory cultures. Finally, access to embryos is difficult, with only a few land-based facilities capable of maintaining spawning broodstocks throughout the world.In the present study we overcome the aforementioned challenges for focal pelagic species that included yellowfin tuna, Southern bluefin tuna (Thunnus maccoyii), and yellowtail amberjack (or kingfish, Seriola lalandi). The yellowfin tuna are the same species that spawn in the Gulf of Mexico, and the other two species are closely related congenerics to T. thynnus and S. dumerili, respectively. Controlled bluefin tuna spawning is exceptionally difficult to achieve in a husbandry facility, and we used the only land-based captive broodstock available in the world for experiments. Similarly, we relied on a commercial broodstock of yellowtail amberjack and a research broodstock of yellowfin tuna, the latter the only worldwide source of fertilized embryos for this species. Embryos were exposed to high-energy water-accommodated fractions (HEWAFs) (20) that generated PAH concentrations and compositional profiles closely matching water samples collected during active MC252 crude oil release phase.     

Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill

Quantitative information regarding the endmember composition of the gas and oil that flowed from the Macondo well during the Deepwater Horizon oil spill is essential for determining the oil flow rate, total oil volume released, and trajectories and fates of hydrocarbon components in the marine environment. Using isobaric gas-tight samplers, we collected discrete samples directly above the Macondo well on June 21, 2010, and analyzed the gas and oil. We found that the fluids flowing from the Macondo well had a gas-to-oil ratio of 1,600 standard cubic feet per petroleum barrel. Based on the measured endmember gas-to-oil ratio and the Federally estimated net liquid oil release of 4.1 million barrels, the total amount of C₁-C₅ hydrocarbons released to the water column was 1.7 × 10¹¹ g. The endmember gas and oil compositions then enabled us to study the fractionation of petroleum hydrocarbons in discrete water samples collected in June 2010 within a southwest trending hydrocarbon-enriched plume of neutrally buoyant water at a water depth of 1,100 m. The most abundant petroleum hydrocarbons larger than C₁-C₅ were benzene, toluene, ethylbenzene, and total xylenes at concentrations up to 78 μg L^-1. Comparison of the endmember gas and oil composition with the composition of water column samples showed that the plume was preferentially enriched with water-soluble components, indicating that aqueous dissolution played a major role in plume formation, whereas the fates of relatively insoluble petroleum components were initially controlled by other processes.     

Forecasting sudden changes in environmental pollution patterns

The lack of reliable forecasts for the spread of oceanic and atmospheric contamination hinders the effective protection of the ecosystem, society, and the economy from the fallouts of environmental disasters. The consequences can be dire, as evidenced by the Deepwater Horizon oil spill in the Gulf of Mexico in 2010. We present a methodology to predict major short-term changes in environmental contamination patterns, such as oil spills in the ocean and ash clouds in the atmosphere. Our approach is based on new mathematical results on the objective (frame-independent) identification of key material surfaces that drive tracer mixing in unsteady, finite-time flow data. Some of these material surfaces, known as Lagrangian coherent structures (LCSs), turn out to admit highly attracting cores that lead to inevitable material instabilities even under future uncertainties or unexpected perturbations to the observed flow. These LCS cores have the potential to forecast imminent shape changes in the contamination pattern, even before the instability builds up and brings large masses of water or air into motion. Exploiting this potential, the LCS-core analysis developed here provides a model-independent forecasting scheme that relies only on already observed or validated flow velocities at the time the prediction is made. We use this methodology to obtain high-precision forecasts of two major instabilities that occurred in the shape of the Deepwater Horizon oil spill. This is achieved using simulated surface currents preceding the prediction times and assuming that the oil behaves as a passive tracer.     

Estimating oil concentration and flow rate with calibrated vessel-mounted acoustic echo sounders

As part of a larger program aimed at evaluating acoustic techniques for mapping the distribution of subsurface oil and gas associated with the Deepwater Horizon-Macondo oil spill, observations were made on June 24 and 25, 2010 using vessel-mounted calibrated single-beam echo sounders on the National Oceanic and Atmospheric Administration ship Thomas Jefferson. Coincident with visual observations of oil at the sea surface, the 200-kHz echo sounder showed anomalously high-volume scattering strength in the upper 200 m on the western side of the wellhead, more than 100 times higher than the surrounding waters at 1,800-m distance from the wellhead, and weakening with increasing distance out to 5,000 m. Similar high-volume scattering anomalies were not observed at 12 or 38 kHz, although observations of anomalously low-volume scattering strength were made in the deep scattering layer at these frequencies at approximately the same locations. Together with observations of ocean currents, the acoustic observations are consistent with a rising plume of small (< 1-mm radius) oil droplets. Using simplistic but reasonable assumptions about the properties of the oil droplets, an estimate of the flow rate was made that is remarkably consistent with those made at the wellhead by other means. The uncertainty in this acoustically derived estimate is high due to lack of knowledge of the size distribution and rise speed of the oil droplets. If properly constrained, these types of acoustic measurements can be used to rapidly estimate the flow rate of oil reaching the surface over large temporal and spatial scales.     

From the Cover: Applications of science and engineering to quantify and control the Deepwater Horizon oil spill

The unprecedented engagement of scientists from government, academia, and industry enabled multiple unanticipated and unique problems to be addressed during the Deepwater Horizon oil spill. During the months between the initial blowout on April 20, 2010, and the final well kill on September 19, 2010, researchers prepared options, analyses of tradeoffs, assessments, and calculations of uncertainties associated with the flow rate of the well, well shut in, killing the well, and determination of the location of oil released into the environment. This information was used in near real time by the National Incident Commander and other government decision-makers. It increased transparency into BP’s proposed actions and gave the government confidence that, at each stage proposed, courses of action had been thoroughly vetted to reduce risk to human life and the environment and improve chances of success.     

Osmotic stress does not trigger brevetoxin production in the dinoflagellate Karenia brevis

With the global proliferation of toxic harmful algal bloom species, there is a need to identify the environmental and biological factors that regulate toxin production. One such species, Karenia brevis, forms nearly annual blooms that threaten coastal regions throughout the Gulf of Mexico. This dinoflagellate produces brevetoxins, which are potent neurotoxins that cause neurotoxic shellfish poisoning and respiratory illness in humans, as well as massive fish kills. A recent publication reported that a rapid decrease in salinity increased cellular toxin quotas in K. brevis and hypothesized that brevetoxins serve a role in osmoregulation. This finding implied that salinity shifts could significantly alter the toxic effects of blooms. We repeated the original experiments separately in three different laboratories and found no evidence for increased brevetoxin production in response to low-salinity stress in any of the eight K. brevis strains we tested, including three used in the original study. Thus, we find no support for an osmoregulatory function of brevetoxins. The original publication also stated that there was no known cellular function for brevetoxins. However, there is increasing evidence that brevetoxins promote survival of the dinoflagellates by deterring grazing by zooplankton. Whether they have other as-yet-unidentified cellular functions is currently unknown.     

From the Cover: Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle

Hydrocarbons are ubiquitous in the ocean, where alkanes such as pentadecane and heptadecane can be found even in waters minimally polluted with crude oil. Populations of hydrocarbon-degrading bacteria, which are responsible for the turnover of these compounds, are also found throughout marine systems, including in unpolluted waters. These observations suggest the existence of an unknown and widespread source of hydrocarbons in the oceans. Here, we report that strains of the two most abundant marine cyanobacteria, Prochlorococcus and Synechococcus, produce and accumulate hydrocarbons, predominantly C15 and C17 alkanes, between 0.022 and 0.368% of dry cell weight. Based on global population sizes and turnover rates, we estimate that these species have the capacity to produce 2–540 pg alkanes per mL per day, which translates into a global ocean yield of ∼308–771 million tons of hydrocarbons annually. We also demonstrate that both obligate and facultative marine hydrocarbon-degrading bacteria can consume cyanobacterial alkanes, which likely prevents these hydrocarbons from accumulating in the environment. Our findings implicate cyanobacteria and hydrocarbon degraders as key players in a notable internal hydrocarbon cycle within the upper ocean, where alkanes are continually produced and subsequently consumed within days. Furthermore we show that cyanobacterial alkane production is likely sufficient to sustain populations of hydrocarbon-degrading bacteria, whose abundances can rapidly expand upon localized release of crude oil from natural seepage and human activities.Hydrocarbons are ubiquitous in the oceans, where natural seepage and human activities are estimated to release between 0.4 and 4.0 million tons of crude oil into the ocean ecosystem annually (1). Even in minimally polluted marine surface waters, alkanes such as pentadecane and heptadecane have been found at concentrations ranging from 2 to 130 pg/mL (2, 3), although their sources remain unclear. A small proportion of alkanes, from 1 to 60 fg/mL, is associated with particulate matter >0.7 µm in diameter (4). Larger amounts may be associated with particulate matter <0.7 µm in diameter, because ocean concentrations are higher than the solubility of pentadecane and heptadecane, which is ∼10 pg/mL and 1 pg/mL, respectively (2). Populations of hydrocarbon-degrading bacteria, referred to as hydrocarbonoclastic bacteria, including many species that cannot use other carbon sources, are present in marine systems and play an important role in turnover of these compounds (5–9). Because obligate hydrocarbon-degrading bacteria are found in waters without significant levels of crude oil pollution, these organisms must use an alternate hydrocarbon source (9–11).Here, we investigate the extent to which cyanobacteria may contribute to these marine hydrocarbon pools. Cyanobacteria (oxygenic photosynthetic bacteria) can synthesize C15 to C19 hydrocarbons via two separate pathways. The first produces alkanes, predominantly pentadecane, heptadecane, and methyl-heptadecane, in addition to smaller amounts of alkenes, via acyl-ACP reductase (FAR) and aldehyde deformylating oxygenase (FAD) enzymes (12). The second pathway generates alkenes, primarily nonadecene and 1,14-nonadecadiene, via a polyketide synthase enzyme (Ols) (13). The abundance and ubiquity of cyanobacteria in the marine environment suggests hydrocarbon production in the oceans could be considerable and broadly distributed geographically (14, 15).We focused our studies on the two most abundant marine cyanobacteria, Prochlorococcus and Synechococcus (16). These genera have estimated global population sizes of 2.9 ± 0.1 × 10²⁷ and 7.0 ± 0.3 × 10²⁶ cells, respectively (14), and are together responsible for approximately a quarter of marine net primary production (14). These are also the only cyanobacterial genera for which global population size estimates have been compiled (14). Although the distribution patterns of both genera overlap (14, 17), Prochlorococcus cells dominate low-nutrient open-ocean areas between 40°N and 40°S and can be found at depths of up to 200 m (16, 18). Synechococcus are more numerous in coastal and temperate regions where conditions and nutrient levels are more variable (14, 16) but are still widely distributed in high abundance.     

Population Genetic Structure of Southern Flounder Inferred from Multilocus DNA Profiles

Determination of stock structure is an important component of fisheries management; incorporation of molecular genetic data is an effective method for assessing differentiation among putative populations. We examined genetic variation in Southern Flounder Paralichthys lethostigma within and between the U.S. South Atlantic and Gulf of Mexico basins to improve our understanding of the scale of population structure in this wide-ranging species. Analysis of amplified fragment length polymorphism (AFLP) fingerprints and analysis of mitochondrial DNA (mtDNA) control region sequences found clear divergence between ocean basins. Based on mtDNA sequences, no genetic differentiation was detected within the U.S. South Atlantic at spatial scales that were broad (among states: North Carolina, South Carolina, Georgia, and Florida) or fine (among estuarine regions within North Carolina). Increased genetic resolution was observed with AFLP fingerprint data, and we found significant subdivision between nearly all Southern Flounder geographic populations, suggesting the presence of finer-scale genetic population structure within the U.S. South Atlantic. However, AFLP genetic cluster analysis also revealed evidence for a high degree of mixing within the Atlantic basin; patterns of variation, which included genetic similarity between South Carolina and Gulf of Mexico samples, were not aligned closely with geography. We examined the partitioning of genetic variation among groups by using analyses of molecular variance and found no evidence that North Carolina Southern Flounder, which are managed on the state level as a unit stock, are differentiated from the remainder of U.S. South Atlantic Southern Flounder. Our findings indicate only weak structure and the potential for basinwide mixing among Atlantic Southern Flounder, suggesting that cooperation among U.S. South Atlantic states will be essential for the effective assessment of stock dynamics and future management plans.     

Environmental and anthropogenic controls over bacterial communities in wetland soils

Soil bacteria regulate wetland biogeochemical processes, yet little is known about controls over their distribution and abundance. Bacteria in North Carolina swamps and bogs differ greatly from Florida Everglades fens, where communities studied were unexpectedly similar along a nutrient enrichment gradient. Bacterial composition and diversity corresponded strongly with soil pH, land use, and restoration status, but less to nutrient concentrations, and not with wetland type or soil carbon. Surprisingly, wetland restoration decreased bacterial diversity, a response opposite to that in terrestrial ecosystems. Community level patterns were underlain by responses of a few taxa, especially the Acidobacteria and Proteobacteria, suggesting promise for bacterial indicators of restoration and trophic status.     

Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism

Marine microalgae support world fisheries production and influence climate through various mechanisms. They are also responsible for harmful blooms that adversely impact coastal ecosystems and economies. Optimal growth and survival of many bloom-forming microalgae, including climatically important dinoflagellates and coccolithophores, requires the close association of specific bacterial species, but the reasons for these associations are unknown. Here, we report that several clades of Marinobacter ubiquitously found in close association with dinoflagellates and coccolithophores produce an unusual lower-affinity dicitrate siderophore, vibrioferrin (VF). Fe-VF chelates undergo photolysis at rates that are 10–20 times higher than siderophores produced by free-living marine bacteria, and unlike the latter, the VF photoproduct has no measurable affinity for iron. While both an algal-associated bacterium and a representative dinoflagellate partner, Scrippsiella trochoidea, used iron from Fe-VF chelates in the dark, in situ photolysis of the chelates in the presence of attenuated sunlight increased bacterial iron uptake by 70% and algal uptake by >20-fold. These results suggest that the bacteria promote algal assimilation of iron by facilitating photochemical redox cycling of this critical nutrient. Also, binary culture experiments and genomic evidence suggest that the algal cells release organic molecules that are used by the bacteria for growth. Such mutualistic sharing of iron and fixed carbon has important implications toward our understanding of the close beneficial interactions between marine bacteria and phytoplankton, and the effect of these interactions on algal blooms and climate.