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Lawrence Berkeley National Laboratory Lawrence Berkeley National Laboratory Lawrence Berkeley National Laboratory Lawrence Berkeley National Laboratory Title Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill Permalink https://escholarship.org/uc/item/8k191344 Author Baelum, J. Publication Date 2012-04-15 DOI DOI:10.1111/j.1462-2920.2012.02780.x Peer reviewed eScholarship.org Powered by the California Digital Library University of California Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill Jacob Bælum1,2, Sharon Borglin1, Romy Chakraborty1, Julian L. Fortney1, Regina Lamendella1, Olivia U. Mason1, Manfred Auer1, Marcin Zemla1, Markus Bill1, Mark E. Conrad1, Stephanie A. Malfatti3, Susannah G. Tringe3, Hoi-Ying Holman1, Terry C. Hazen1, and Janet K. Jansson1,3* 1 MS 70A-3317, 1 Cyclotron Rd., Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA 2 The Geological Survey of Denmark and Greenland, Øster Voldgade 10, 1350 Copenhagen, Denmark 3 Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA * Corresponding author phone: 1-510-486-7487; e-mail: [email protected]; fax: 1-510- 486-7152 Running title: Enrichment of oil degraders from Gulf of Mexico 1 Summary 2 The Deepwater Horizon oil spill resulted in a massive influx of hydrocarbons into the 3 Gulf of Mexico (the Gulf). To better understand the fate of the oil, we enriched and 4 isolated indigenous hydrocarbon-degrading bacteria from deep, uncontaminated waters 5 from the Gulf with oil (Macondo MC252) and dispersant used during the spill 6 (COREXIT 9500). During 20 days of incubation at 5ºC, CO2 evolution, hydrocarbon 7 concentrations, and the microbial community composition were determined. 8 Approximately 60% to 25% of the dissolved oil with or without COREXIT, respectively, 9 was degraded, in addition to some hydrocarbons in the COREXIT. FeCl2 addition 10 initially increased respiration rates, but not the total amount of hydrocarbons degraded. 11 16S rRNA gene sequencing revealed a succession in the microbial community over time, 12 with an increase in abundance of Colwellia and Oceanospirillales during the incubations. 13 Flocs formed during incubations with oil and/or COREXIT in the absence of FeCl2. 14 Synchrotron radiation-based Fourier transform infrared (SR-FTIR) spectromicroscopy 15 revealed that the flocs were comprised of oil, carbohydrates and biomass. Colwellia were 16 the dominant bacteria in the flocs. Colwellia sp. strain RC25, was isolated from one of 17 the enrichments and confirmed to rapidly degrade high amounts (approximately 75%) of 18 the MC252 oil at 5ºC. Together these data highlight several features that provide 19 Colwellia with the capacity to degrade oil in cold, deep marine habitats, including 20 aggregation together with oil droplets into flocs and hydrocarbon degradation ability. 21 22 23 Introduction 24 On April 20, 2010, high-pressure oil and gas caused the Deepwater Horizon drilling rig in 25 the Gulf of Mexico to explode resulting in the second largest marine oil spill in the 26 history of petroleum industry. It has been estimated that ~4.1 million barrels of light 27 crude oil and natural gas leaked into the Gulf from the Macondo well (MC252) during 28 the ~3 months before the well head was capped (OSAT, 2010). Primarily in an attempt to 29 improve safety for surface operating vehicles, ~1.8 million gallons (~37,500 barrels) of 30 the chemical dispersant COREXIT (mainly 9500, but also 9527 formulation) was applied 31 to the Gulf surface as well as directly into the wellhead at 1500 meters below surface 32 level (mbsl; 9500 only). Very little is known about the effects and persistence of 33 COREXIT in the environment, including its impact on indigenous microbes in the Gulf 34 (Judson, et al., 2010). 35 During the spill, hydrocarbon concentrations varied from 100% at the source to 36 undetectable with increasing distance from the wellhead. During exploratory and 37 surveillance cruises conducted for the US Coast Guard, National Oceanic and 38 Atmospheric Administration (NOAA), and the US Environmental Protection Agency 39 (EPA), a plume or cloud of dispersed MC252 crude oil was detected at 1100-1220 mbsl 40 at distances up to 35 km from the wellhead (Camilli, et al., 2010). The plume is thought 41 to have formed due to application of COREXIT at the wellhead and a combination of 42 physical and chemical properties at 1100 mbsl depth (e.g. pressure, temperature (~5ºC), 43 and salinity (Adcroft, et al., 2010, Dasanayaka & Yapa, 2009, Yapa, et al., 2008), that 44 resulted in the oil attaining neutral buoyancy at this depth. During the ongoing release of 45 oil several research groups reported the presence of the plume, but after the wellhead was 46 capped the plume was no longer detectable (OSAT, 2010). 47 Several reports have provided strong evidence that microbial processes were a 48 key factor for degradation and removal of oil from the plume (OSAT, 2010). For 49 example, Hazen et al. (2010) reported a shift in the composition of the microbial 50 community in the deep-sea plume within one month of the spill (May 2010). They found 51 that sequences corresponding to Oceanospirillales dominated in the oil plume, but that 52 they were rare in uncontaminated water at the same depth. Later sampling of the plume in 53 June, 2010 reported that sequences representative of Cycloclasticus and Colwellia were 54 dominant, together accounting for more than 95% of the sequence data (Valentine et al., 55 2010). Recently, Redmond & Valentine (2011) reported that Colwellia sequences 56 increased in abundance during enrichment on crude oil at cold temperatures (4 °C) 57 compared to warmer (20 °C) incubation conditions and suggested that temperature was a 58 major determinant in selection of this group of microorganisms. 59 Here we aimed to study the succession of the indigenous microbial community 60 and the formation of microbial flocs in deep-sea water from the Gulf of Mexico during 61 laboratory enrichments at cold temperature (5°C) and with high concentrations of MC252 62 oil and COREXIT. We also aimed to select and isolate specific members of the microbial 63 community having the capability to degrade oil in the presence or absence of dispersant. 64 The source of inoculum was uncontaminated seawater collected from the Gulf of Mexico 65 during the Deepwater Horizon oil spill at the depth of the reported hydrocarbon plume 66 (1100 mbsl). We also looked at the impact of Fe2+ on the degradation rates because iron 67 was reported to be a potentially limiting nutrient for microbial growth in the water 68 column (Hazen, et al., 2010, Lu, et al., 2011, OSAT, 2010). 69 During the enrichments the community composition was monitored by 454 70 pyrotag sequencing of 16S rRNA genes. We also monitored respiration and degradation 71 of oil and COREXIT during the incubations. These experiments enabled us to gain a 72 better understanding of the pattern of microbial succession, and the response of specific 73 microbial populations when exposed to high concentrations of hydrocarbons such as 74 occurred during the Deepwater Horizon oil spill or that naturally occur from oil seeps on 75 the ocean floor. 76 77 Results 78 Respiration during enrichments 79 Microbial populations in water collected from the deep-sea in the Gulf of Mexico 80 were enriched to grow on and degrade high concentrations of Macondo MC252 oil, in the 81 presence or absence of the dispersant, COREXIT 9500 at low temperature (5°C). 82 Additional treatments included Fe amendment and sterile controls. As a dissolved oxygen 83 concentration of 6.07 mg/L was measured on site (Hazen, et al., 2010), our experiments 84 were done under aerobic conditions. Dissolved oxygen concentrations measured on 0, 5, 85 and 20 days of incubation were 8.4, 7.5, and 6.1 mg/L, respectively. 86 During the enrichments we observed significant differences (t-test, P<0.05) in CO2 87 evolution patterns between the different treatments (Fig. 1a). There was a substantial 88 increase in CO2 evolution in the enrichments containing oil and/or COREXIT compared 89 to sterile controls. In the enrichments with oil alone and oil+Fe, the cumulative CO2 90 evolution during the 20-day incubation period was in the range of 2.8-3.0 mg CO2, and in 91 those with COREXIT in the range 4.4-4.9 mg CO2, regardless of the presence of oil (Fig. 92 1a). In the presence of FeCl2 there was an immediate onset of CO2 evolution, while in the 93 enrichments without FeCl2, there was a lag phase of ~6 days before CO2 evolution 94 commenced. However, regardless of the addition of FeCl2, the total amount of CO2 that 95 accumulated after 20 days was similar. 96 97 Degradation of Macondo crude oil 98 During the incubations we determined the concentration of dissolved crude oil 99 (measured as total petroleum hydrocarbons, TPH) by extracting aliquots of the seawater 100 and analyzing by GC-FID as described below. In the treatments with oil and no 101 COREXIT, oil adhered to the sides of the bottles, reducing the amount in the seawater to 102 approximately 30% of the initial concentration of 100 ppm. In samples with COREXIT 103 more of the oil was dissolved; ∼70% of the initial concentration (Fig. 1b), as expected 104 because COREXIT is a dispersant. After 5 days of incubation 25% of the dissolved oil 105 was degraded in samples with oil alone and 40% in samples with oil and COREXIT. 106 After 20 days no additional oil was degraded in the samples with oil alone, but 60% had 107 been degraded in samples with oil and COREXIT (for mass balances see supplemental 108 information Fig. S2). While the oil degradation was reported as TPH, the majority of 109 compounds lost were straight chain alkanes, which were predominant components of the 110 MC 252 source oil.
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