Oil Biodegradation in Deep Marine Basins
Nine important hydrocarbon (oil) basins where offshore petroleum leases have been licensed are compared. These nine basins (Gulf of Mexico, Eastern Mediterranean’s Nile Deep-Sea Fan, Central Mediterranean and the Sirte Basin, North Sea, Caspian Sea, Angola, Trinidad and Tobago, Great Australian Bight, and Brazil’s Amazonian Deep-Sea Basin) are geographically separated and are impacted by very different water masses. The geochemical parameters of these basins are quite distinct, for example, salinities ranging from 39 psu in the Eastern Mediterranean to 12 psu in the Caspian. Additionally, parameters like temperatures of the bottom water are also very distinct, with the temperature in the deep water of the Eastern Mediterranean being between 12 °C and 14 °C and the temperature of the deep water in the North Sea being −2 °C. Each basin represents a unique ecosystem in which distinct microbes may thrive. These distinct environmental parameters may act to constrain the extent of hydrocarbon degradation in these basins. Another potential constraint on hydrocarbon degradation is the extent of natural hydrocarbon seeps in the area. Though many basins have similar if not 16S rRNA identical strains of oil-degrading bacteria, Colwellia psychrerythraea from different basins showed that a mixture of natural selection and neutral evolution has contributed to the divergence of these. Most if not all deep ocean basin microbial communities are dominated by Thaumarchaeota below 200 m. These microaerophilic, ammonium oxidizer, psychrophiles are very adapted to an oligotrophic lifestyle, and though many in this group will degrade oil, they are rapidly outcompeted by other bacteria in oil or high hydrocarbon intrusions, thus the virtual “canary in the coal mine.” Cometabolic biodegradation of oil is well documented but could be an important natural attenuation mechanism for oil in deep marine basins with episodic methane seeps. Microbial community structure can also predict concentrations of oil in deep basins. Many other synergistic effects require more research in environmental systems biology in deep marine basins.
As sources of new oil reservoirs on land became scarcer over the last 20 years, offshore oil production had dramatically increased. Though the production costs were much greater than wells on land, since the oil reservoirs being tapped were deeper, the value of the product was higher due to its lighter nature and higher value as fuel. However, the DWH blowout in deep water created a cautionary reevaluation and more risk assessment studies. In addition, unconventional oil production and shale gas production increased by more than 702% since 2007. This in turn has caused many oil companies to abandon offshore oil production in deep marine basins, including leases and exploration. “Global oil discoveries fell to a record low in 2016 as companies continued to cut spending and conventional oil projects sanctioned were at the lowest level in more than 70 years,” according to the International Energy Agency (IAE 2017). “The offshore sector, which accounts for almost a third of crude oil production and is a crucial component of future global supplies, has been particularly hard hit by the industry’s slowdown. In 2016, only 13% of all conventional resources sanctioned were offshore, compared with more than 40% on average between 2000 and 2015” (IAE 2017).
2 Deep Marine Bacterial Oil Degraders
The Caspian Sea has many natural seeps and oil production throughout the basin. It is estimated that the Caspian receives between 70 and 90 tonnes of petroleum each year (Chicherina et al. 2004). Total petroleum levels in the Caspian range between 0.067 and 2 mg/L (Korshenko and Gul 2005). The highest levels of petroleum hydrocarbons were found in the Southern Caspian. These concentrations range from 0.17 to 0.07 mg/L. Caspian Sea water from 200–600 m is dominated by Betaproteobacteria, Gammaproteobacteria, Deltaproteobacteria, Alphaproteobacteria, Actinobacteria, and Thaumarchaeota. Fungi capable of oil degradation have also been isolated from the Caspian Sea water column (Salmanov 2006; Lein et al. 2010). Studies on the Caspian Sea indicate that the surface of deepwater sediments with low oxygen levels was dominated by Gammaproteobacteria; however, surface sediments with bottom waters under hypoxic conditions were dominated by Deltaproteobacteria. The ammonia-oxidizing Thaumarchaeota was dominant in all surface sediments (Mahmoudi et al. 2015).
Eastern Mediterranean’s Nile Deep-Sea Fan has numerous natural hydrocarbon seeps (Heijs et al. 2008; Mastalerz et al. 2009; Omoregie et al. 2009; Felden et al. 2013). Deep water from 400 to 1200 m is dominated by SAR406, Gammaproteobacteria, Deltaproteobacteria, Alphaproteobacteria, Actinobacteria, Chloroflexi, and Thaumarchaeota (Techtmann et al. 2015). The microbial community in the deep water was significantly correlated with inorganic phosphate, silicate, nitrate, and depth. Deep sediments were dominated by Actinobacteria, Bacilli, Chloroflexi, Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Deltaproteobacteria, and Epsilonproteobacteria and the archaea Methanosarcinales, Thermoplasmales, Halobacteriales, and Crenarchaea (Heijs et al. 2008). Sulfate reduction, aerobic and anaerobic methanotrophy, aerobic sulfide oxidation, and aerobic and anaerobic heterotrophy were the dominant metabolic processes in the deep sediment (Heijs et al. 2008).
The Central Mediterranean and the Sirte Basin were largely the same for both water and sediment microbial communities as the Eastern Mediterranean. However, the microbial community structure in the water column was driven by dissolved oxygen, temperature, and salinity (Techtmann et al. 2017). The levels of hydrocarbon-degrading bacteria in coastal waters at locations in the Mediterranean have been determined to be 10–102 cells/ml of water (Youssef et al. 2010). In many locations, the addition of oil enriches a robust community of oil-degrading microbes (Moursy and El-Abagy 1982; Santas et al. 1999; Zrafi-Nouira et al. 2009; Ibraheem 2010; Youssef et al. 2010; Chekroud et al. 2011; Farag and Soliman 2011). Cyanobacteria have been found to be a part of this community (Ibraheem 2010). The authors suggest that their data supports either the ability of these cyanobacteria to degrade hydrocarbons or a mutualism between these cyanobacteria and aerobic hydrocarbon-degrading bacteria. This community also contains hydrocarbon-degrading fungi from the genus Candida (Farag and Soliman 2011).
The Great Australian Bight (GAB) has only a few natural seeps but is of interest for oil production (Logan et al. 2010). Over the years, there have been a number of studies aimed at identifying the presence of hydrocarbon seeps within Australia’s margins (Logan et al. 2010). To date, the only naturally occurring hydrocarbon seeps identified are located in Northern Australia’s carbonate-rich shelf in the Timor Sea (Rollet et al. 2006; Wasmund et al. 2009; Logan et al. 2010). In Southern Australia, the presence of naturally occurring bitumen asphaltites within the GAB suggests that a naturally occurring seep may be present off of Australia’s southern margin. However, there is no direct evidence and despite surveys of the area, no natural seeps within the GAB have been recorded (Struckmeyer et al. 2002; Logan et al. 2010). The GAB is very oligotrophic and one of the deepest basins being considered for petroleum exploration. In the water column, the Thaumarchaeota are the dominant microorganism below 185 m in depth (Techtmann et al. 2017). Other groups found are Prochlorococcus, Synechococcus, SAR11, Rhodobacteriales, Oceanospirillales, Alteromonadales, and Bacteroidetes (Wilkins et al. 2013). Microbial diversity in sediments near a methane seep has revealed novel aerobic methanotroph diversity (Wasmund et al. 2009). Within hydrocarbon seeps in the Timor Sea, phylogenetic analysis revealed the presence of sequences affiliated with Gammaproteobacteria, Deltaproteobacteria, Alphaproteobacteria, Acidobacteria, Bacteroidetes, Firmicutes, and Nitrospira. Additionally, sequences associated with aerobic methanotrophs were identified, while sequences related to methanotrophic Archaea were found to be absent. Analysis of genes within the porewater revealed the absence of the methanogenic functional gene, methyl coenzyme M reductase, thus providing further evidence for the lack of methanotrophic assemblages at the seeps (Wasmund et al. 2009).
The Angola Basin (OSA) is a deepwater upwelling basin with a significant number of natural oil seeps (Berger et al. 1998). Crenarchaeota are the most dominant group of microbes in OSA below 400 m and are common in low-nutrient deep ocean environments worldwide. The Crenarchaeota are generally microaerophiles that are known to be ammonium oxidizers, which gives them a competitive advantage in low-nutrient environments. The microbial community in the OSA is driven by total organic carbon, dissolved oxygen, salinity, and temperature (Hazen et al. 2016). Other microbes in the water included SAR406, Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Deltaproteobacteria, Euryarchaeota, and Thaumarchaeota. The dominant sediment organisms are Gammaproteobacteria, particularly psychrophilic Enterobacteriaceae, Alteromonadaceae, Oceanospirillaceae, and Legionellaceae (Schauer et al. 2010). Other proteobacteria, Chloroflexi and Planctomyces, were also found in the sediment.
In the North Sea temperature, salinity, and availability of nutrients are some of the drivers that can dictate the microbial community structure. Often in marine systems, movement of waters by currents and tides and stratification help to determine these factors. In the North Sea, the loosely defined regions of the shallow continental shelf of the southern and central North Sea, the Norwegian Trench, and the Faroe-Shetland Channel have distinct current systems and vertical stratification. Natural hydrocarbon seeps in the North Sea as well as anthropogenic inputs of hydrocarbons contribute the overall hydrocarbon load of the Sea. Riverine inputs carry with it anthropogenic hydrocarbons and are estimated to contribute between 40 and 80 kilotons of petroleum hydrocarbon per year into the North Sea (Bedborough et al. 1987). Another significant source of anthropogenic hydrocarbons is the offshore oil and gas industry. This industry has had a major presence in the North Sea since the 1960s. Some studies (Bedborough et al. 1987) estimate that the offshore petroleum industry contributes around 23 kilotons of petroleum per year to the North Sea. The phytoplanktonic communities of the North Sea have been the subjects of a large number of studies (Dale et al. 1999; Riegman and Kraay 2001; Kuipers et al. 2003; Loder et al. 2012). Another study examining the long-term shifts in community structure examined the microbial community of the Helgoland Roads during August over the course of a half-century (Vezzulli et al. 2012). As in other studies, this report finds that Alpha- and Gammaproteobacteria dominate the community over the course of these decades. Oceanospirillaceae, Halomonadaceae, and Alteromonadales increase over time. The most significant increase that was observed is in the Vibrio spp. This increase in Vibrios is strongly correlated with sea surface temperature. Therefore, the authors conclude that the warming of sea surface temperatures has resulted in drastic shifts in the microbial communities of the North Sea. The bacterial and archaeal communities of the North Sea are key players in various geochemical cycles within the sea. In the Tommeliten seep, no methanotrophs were found. However, other organisms were found that might serve as functional analogs for the degradation of complex organic matter. Sequences for a relative of Desulfitobacterium anili were found at the Tommeliten site. This organism has previously been shown to oxidize various hydrocarbons such as naphthalene and xylene (Widdel et al. 2007). In addition, a 16 s rDNA clone for a member of the Oceanospirillales was recovered from the Tommeliten site.
The coast of Trinidad and Tobago is very complex environment where many water masses interact. This location is increasingly becoming an important region for oil and gas production. The complex environment of this region makes it an interesting site to examine the microbial communities present in the waters and sediments and their potential to degrade hydrocarbons. Some of the microbiological work in the region has involved examining the microbes that colonize the unique gradients associated with the riverine inputs into the Atlantic from the Orinoco and the Amazon Rivers. One such paper examines the levels and turnover times of methane (CH4) and carbon monoxide (CO) in the waters of the Caribbean Sea surrounding Trinidad and Tobago (Jones and Amador 1993). In rivers methane is produced microbially by methanogenic archaea, and CO is produced primarily by the photooxidation of organic matter. CO is subsequently consumed through microbial oxidation of CO. An interesting trend was seen in the Gulf of Paria, where the CO and CH4 concentrations reached a local maximum. This is most likely due to effects on the flow of riverine waters into the gulf. This work confirms that the waters around Trinidad and Tobago are highly influenced by inputs of both nutrients and organic matter from the Orinoco River. A large number of mud volcanoes have been discovered near Trinidad and Tobago in the Barbados Prism (Biju-Duval et al. 1982; Brown and Westbrook 1987, 1988; Brown 1990; Griboulard et al. 1991; Deville et al. 2003). These mud volcanoes are rather randomly distributed along the continental slope (Deville et al. 2006, 2010). These mud volcanoes have been shown to exude both methane and higher hydrocarbons (Le Pichon et al. 1990a, b; Henry et al. 1996). The microbiology of deep sediments adjacent to Trinidad and Tobago was investigated by Guezennec and Fiala-Medioni (1996). They used phospholipid ester-linked fatty acids (PLFA) to examine the bacterial abundance and diversity of a mud volcano in the Barbados trench near Trinidad and Tobago. Prior to this work, white and reddish mats were observed near these seep sites indicative of some bacterial colonization (Le Pichon et al. 1990a). PLFA analysis estimated the cell numbers in these mud volcanoes to be 1.5 × 109 cell/g of sediment. These cell numbers are similar to others reported in nearby sediments of the Venezuelan Basin (5 × 108 cells/g). The lipid profiles of sites near the white and reddish mats suggested the presence of sulfur-oxidizing bacteria. Further, lipid characteristics of both type I and type II methanotrophs were common at all sites sampled. This would follow the high levels of methane present at these sites. The authors conclude that type I methanotrophs are more abundant than type II in all of the sediments. Other lipids commonly found in both sulfate-reducing bacteria as well as alkane-degrading bacteria were found in these sediments. Archaeal lipids potentially belonging to methanogens were also found in these sediments. While this study does shed some light on the groups of bacteria present in these mud volcanoes, further work needs to be done to characterize these communities. For example, one of the groups of lipids found at high levels could either be contributed from sulfate-reducing bacteria or alkane-degrading bacteria.
The Amazonian Deep-Sea Basin brings distinct hydrographic and geochemical features to the waters around Brazil and has a large effect on the microbial communities present in these waters. In particular the role that river inputs have on these waters drastically affects the microbial communities present. The complex water masses in the deep water also harbor unique niches for microbes to flourish. Amazonian Deep-Sea Basin water contained oil degraders in the bacteria (Alteromonadaceae, Colwelliaceae, and Alcanivoracaceae), archaea (e.g., Halobacteriaceae, Desulfurococcaceae, and Methanobacteriaceae), and eukaryotic microbes (e.g., Microsporidia, Ascomycota, and Basidiomycota) (Campeao et al. 2017). The sediments off the coast of Brazil are relatively unexplored in terms of their microbial diversity. Despite the active oil and gas industry, which has characterized many of the seafloor and sub-seafloor features, the microbial community of the seafloor is relatively unknown. Microbes have been shown to be present in relatively high numbers (Cragg et al. 1997). Work associated with the Ocean Drilling Program reported bacterial cell numbers around 109 cells/g of sediment in the surface sediments and decreasing to 106 cells/g in the deeper sediments. Due to the oligotrophic nature of the open ocean water, oxygen is able to penetrate fairly deeply into the sediments of this region (Wenzhofer et al. 2001). One study characterized the hydrocarbon-degrading community associated with sediments impacted by a catastrophic oil spill in the Guanabara Bay (Brito et al. 2006). Thirty-two bacterial strains were isolated from oil-enriched mesocosms of Guanabara Bay sediment. The majority of these strains were Alpha- and Gammaproteobacteria. Many of these strains were related to Marinobacter spp. and Alcanivorax spp. The Alphaproteobacteria were shown to be able to degrade many of the branched chain hydrocarbons. Another study investigated various methods to stimulate hydrocarbon degradation in coastal sediments (Silva et al. 2009). In these sediments, hydrocarbon degraders were shown to be a significant proportion of the heterotrophic bacterial population. The addition of fertilizer and biosurfactant helped to stimulate the removal of hydrocarbons from this system.
3 Colwellia psychrerythraea in Deep Marine Basins
Colwellia psychrerythraea are often found in cold, oil-contaminated marine environments both in the deep, near shore, and sediment. Recent in-depth genomic and phenotypic studies of identical isolates from distant basins suggest that even when they show the same 16S rRNA identity, they show differential salt tolerance and distinct carbon source utilization (Techtmann et al. 2016). Differences in genomic content were also shown to encode for different functional capacity. Large segments of the genome appear to be acquired by horizontal gene transfer. Some of these genes confer increased functionality and selective advantage; however, the majority of differences do not appear to be related to adaptation to different environmental lifestyles. This suggests that a mixture of natural selection and neutral evolution has contributed to the divergence of these organisms and the great genetic and phenotypic diversity present within this species. This observation may well be the norm for oil degraders rather than the exception.
4 Thaumarchaeota in Deep Marine Basins (Canary in the Coal Mine)
The Thaumarchaeota dominate the microbial community in the water column in nearly all deep basins that have been studied. This is predominantly because these psychrophilic, microaerophilic, ammonia-oxidizers are very adapted to the oligotrophic environment that dominates the depths of these basins. Some Thaumarchaeota have also been reported to degrade oil at low concentrations. Recent studies of four of these basins demonstrated that there were significant differences in the abundance and diversity of Thaumarchaeotes between these four basins and that their distribution showed biogeographic patterning (Techtmann et al. 2017). These studies have also demonstrated that oil and other hydrocarbons will cause the Thaumarchaeotes to disappear in the water column and sediments since they cannot compete with other oil degraders. Thus, disappearance of Thaumarchaeotes in deep marine basin water columns could be a good indicator of oil and/or hydrocarbon presence, i.e., “canary in the coal mine.”
5 Cometabolic Biodegradation of Oil
The aerobic cometabolic biodegraders are dependent upon oxygenases, e.g., methane monooxygenase, toluene dioxygenase, toluene monooxygenase, and ammonia monooxygenase. These enzymes are extremely strong oxidizers, e.g., methane monooxygenase is known to degrade over 1000 different compounds. However, like any bioremediation process, the proper biogeochemical conditions are necessary to maximize and maintain biodegradation, e.g., maintaining oxygen levels or other terminal electron acceptors that the cometabolic biodegrader is dependent (Hazen 1997; Hazen et al. 2016), and Chapter in this book on Cometabolic Bioremediation. In addition, cometabolic biostimulation may require pulsing of electron donor or electron acceptor to reduce competitive inhibition between the substrate the microbe can use and the contaminant. Pulsing of methane was found to significantly improve biodegradation of TCE rates by methanotrophs (Hazen 2010). Indeed, during the Deepwater Horizon (DWH) leak (Hazen et al. 2010), there was evidence that in the Gulf of Mexico where episodic releases of methane have occurred for millions of years from natural seeps, this pulsing of methane may be degrading oil and other organics via cometabolic biodegradation. The methane oxidizers bloomed during the DWH leaked above 400 m once the well was capped (Reddy et al. 2012; Redmond and Valentine 2012; Dubinsky et al. 2013). This suggests that intrinsic cometabolic bioremediation or cometabolic natural attenuation may be a serious phenomenon in the ocean (Stackhouse et al. 2017). Methanotrophs, methane-oxidizing bacteria, oxidize methane via a series of enzymes that are unique to this group. The primary enzyme in this oxidation chain is methane monooxygenase. Methane monooxygenase is an extremely powerful oxidizer, thus giving it the capability of oxidizing a wide variety of normally recalcitrant compounds including oil (Cardy et al. 1991). See Cometabolic Bioremediation in this book.
6 Biogeochemistry and Oil Biodegradation
Physical/chemical comparison of deep basin with oil biodegradation
Great Australian Bight
Gulf of Mexico
Dissolved oxygen (mg/L)
7 Environmental Systems and Synergistic Effects in Deep Marine Oil Biodegradation
Synergistic effects that impact biodegradation of oil. (After Hazen et al. 2016)
Factor working synergistically
Impact on biodegradation
Chemical dispersants + mineral fines
Individually each will promote dispersion of the oil. Combined, the formation and transfer of oil from the surface into the water column is enhanced
Autoinoculation + “memory response” of hydrocarbon degraders
Introduction of hydrocarbons to previously exposed water parcels leads to an increase in microbial abundance and accelerated hydrocarbon biodegradation
Oil droplet size + dispersion + biodegradation rates + dissolution
Enhances biodegradation, dissolution, and dispersion rates of oil hydrocarbons
Cometabolic biodegradation + dispersion + secondary electron donors
Enhances biodegradation, dissolution, and dispersion rates of oil hydrocarbons even when the oil itself cannot be a suitable electron donor
Biosurfactants from multiple microorganisms
Enhances bioavailability of poorly soluble compounds
8 Research Needs
To avoid and properly remediate disasters like the Deepwater Horizon spill, we need much more in-depth studies at an environmental systems biology level. This includes better models that take into account psychrophiles that can degrade oil and would not be predicted by simple Q10 formulas. More studies are also needed on dispersant usage with particular attention to realistic concentrations. On board ship studies and close attention to bottle effect, temperature and pressure have been found to critically effect conclusions of studies. The resources for doing these studies in deep basins are exceptionally high and need government commitments long term with a dynamic field test plan and experienced personnel for rapid deployment for any future spills.
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