Hydrocarbon-Degrading Microbial Communities Are Site Specific, and Their Activity Is Limited by Synergies in Temperature and Nutrient Availability in Surface Ocean Waters

Abstract

The objective of this study was to quantify the potential for hydrocarbon biodegradation in surface waters of three sites, representing geographic regions of major oil exploration (Beaufort Sea in the Arctic, northern Gulf of Mexico [GOM], and southern GOM), in a systematic experimental design that incorporated gradients in temperature and the availability of major nutrients. Surface seawater was amended in microcosms with Macondo surrogate oil to simulate an oil slick, and microcosms were incubated, with or without nutrient amendment, at temperatures ranging from 4 to 38^ºC. Using respiration rate as a proxy, distinct temperature responses were observed in surface seawater microcosms based on geographic origin; biodegradation was nearly always more rapid in the Arctic site samples than in the GOM samples. Nutrient amendment enhanced respiration rates by a factor of approximately 6, stimulated microbial growth, and generally elevated the taxonomic diversity of microbial communities within the optimal temperature range for activity at each site, while diversity remained the same or was lower at temperatures deviating from optimal conditions. Taken together, our results advance the understanding of how bacterioplankton communities from different geographic regions respond to oil perturbation. A pulsed disturbance of oil is proposed to favor copiotrophic r-strategists that are adapted to pointed seasonal inputs of phytoplankton carbon, displaying carbon and nutrient limitations, rather than oil exposure history. Further understanding of the ecological mechanisms underpinning the complex environmental controls of hydrocarbon degradation is required for improvement of predictive models of the fate and transport of spilled oil in marine environments.IMPORTANCE The risk of an oil spill accident in pristine regions of the world's oceans is increasing due to the development and transport of crude oil resources, especially in the Arctic region, as a result of the opening of ice-free transportation routes, and there is currently no consensus regarding the complex interplay among the environmental controls of petroleum hydrocarbon biodegradation for predictive modeling. We examined the hydrocarbon biodegradation potential of bacterioplankton from three representative geographic regions of oil exploration. Our results showed that rates of aerobic respiration coupled to hydrocarbon degradation in surface ocean waters are controlled to a large extent by effects of temperature and nutrient limitation; hydrocarbon exposure history did not appear to have a major impact. Further, the relationship between temperature and biodegradation rates is linked to microbial community structure, which is specific to the geographic origin.

Keywords: biodegradation; hydrocarbons; microbial communities; nutrients; oil; temperature.

FIG 1

Biodegradation rates, as determined by carbon dioxide accumulation (upper), and estimated maximum respiration rates (lower) according to temperature and nutrient amendment in microcosms of surface seawater. Scatterplots show average values from triplicate measurements. Error bars indicate standard deviations.

FIG 2

Beta (a) and alpha (b) diversity, determined for microbial communities in seawater microcosms, according to temperature and nutrient amendment. Beta diversity is displayed as the Bray-Curtis distance metric on a nonmetric multidimensional scaling (NMDS) plot, and alpha diversity is shown as Shannon entropy. Boxplots show average values of triplicate samples. Error bars indicate standard deviations. NON and NP refer to the unamended and nutrient-amended treatments, respectively.

FIG 3

Microbial community compositions in surface seawater microcosms from CB2 (upper), DWH01 (middle), and IXTOC01 (lower) sites. Barplots show the mean relative abundance of triplicate microcosms. Taxa are grouped at the genus level, and relative abundance was calculated relative to total sequences retrieved.