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 º C. 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.

Niche Partitioning between Coastal and Offshore Shelf Waters Results in Differential Expression of Alkane and Polycyclic Aromatic Hydrocarbon Catabolic Pathways

“…Interestingly, patterns in the taxonomic diversity of expressed hydrocarbon degradation genes did not vary substantially between environments, indicating that some aspects of the response of microbial communities in marine surface waters to oil or chemically dispersed oil exposure may be common between locales. Overall, these findings highlight that natural remediation processes such as microbial biodegradation are not uniform across different ocean biomes ( 36 ) and reinforce the need for a better understanding of the spatial and temporal variances in natural oil remediation processes.…”

Microbial genomics of the global ocean system

“…Usually present in low numbers, oil-degrading species can rapidly reproduce, going from low abundance or even undetectable levels to a substantial and metabolically active community when exposed to oil (Kleindienst et al, 2015a). However, growth rates and response times will vary with environmental (physical, chemical, and biological) parameters (Huettel et al, 2018;Sun and Kostka, 2019).…”

“…• Environmental Conditions: Hydrocarbon degradation is a respiration process, and like all biological processes, it is limited by temperature, the supply of oxygen and major nutrients, and other environmental parameters (Head et al, 2006;Redmond and Valentine, 2012;Rodriguez-R. et al, 2015;Fernandez-Carrera et al, 2016;Sun and Kostka, 2019). For example, petroleum hydrocarbons are generally rich in carbon and poor in major nutrients (e.g.…”

A Rotational Slurry Bioreactor Accelerates Biodegradation of A-Fuel in Oil-Contaminated Soil Even under Low Temperature Conditions

“…Bioaugmentation with oil-degrading bacteria has been used as an effective treatment to clean up the contaminated soil [3][4][5]. However, the certainty and efficiency of bioaugmentation is not necessarily stable, because various environmental conditions, including soil composition, water content, temperature, and indigenous microbes, influence the feasibility of this treatment [6][7][8]. Among these conditions, temperature was one of the most important factors, because the microbial process could be further slowed down in cooler or cold environments [7,8].…”

“…However, the certainty and efficiency of bioaugmentation is not necessarily stable, because various environmental conditions, including soil composition, water content, temperature, and indigenous microbes, influence the feasibility of this treatment [6][7][8]. Among these conditions, temperature was one of the most important factors, because the microbial process could be further slowed down in cooler or cold environments [7,8]. Therefore, the isolation and usage of microbial degraders adapted to cold environments have been performed in several reports [9][10][11][12][13][14][15].…”