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5.1 Introduction

The cold waters and harsh environmental conditions in the Arctic have led some investigators to conclude that spilled oil will be more recalcitrant and remain in the environment for longer periods of time than oil spilled in less harsh environments. Other investigators have concluded that the microorganisms in the Arctic are adapted to those conditions and rapidly respond to spilled oil. The objective of this document is to examine experimental evidence from peer-reviewed literature that addresses these conclusions and identify areas of additional research. 

This chapter focuses on biodegradation of oil spilled into the marine Arctic environment. The state-of-knowledge will be summarized, and main uncertainties that need further addressing will be highlighted. In this summary we also describe some of the specific conditions that organisms involved in biodegradation processes encounter in the Arctic environment but not at lower latitudes. These differentiating conditions, which may affect biodegradation rates and capabilities in the Arctic, include generally low near-surface temperatures, ice coverage and (in open water) extreme fluctuations in the photoperiod during the Arctic summer and winter. 

The risk of oil pollution in the Arctic is relevant to both marine and terrestrial environments. The Arctic marine environment may be influenced by recently discovered oil and gas deposits, together with the potential for increased traffic attributable to shipping lanes made possible by historically low summer ice cover. The terrestrial environments may be exposed to pollution risk, for instance, from oil transport pipeline systems and other land-based activities. In this review we will focus on the marine environments, although references will also be made to terrestrial studies, when relevant. 

Oil compounds can be degraded by a variety of prokaryotic and eukaryotic organisms. After uptake in eukaryotic macro-organisms, provided they are at sub-lethal or sub-inhibitory concentrations, the compounds may be transformed by the metabolic apparatus, bio-accumulated, or removed through fecal excretion. Despite the range of organism types that can act on oil, however, the microbial communities are regarded as the main source for biological degradation of marine contamination. This perspective is based on the large concentrations of microorganisms, large surface-to-volume ratios and their rapid responses to the situation. This section will therefore focus on the microbial populations and their responses to possible oil discharges in the Arctic marine environment. 

Based on sequencing studies of the 16S rRNA gene, in the mid-1970s Carl Woese and colleagues separated living organisms into the domains Eukarya, Archaea and Bacteria (Woese et al. 1990). Microorganisms are present in all three domains. The bacteria and archaea are all microorganisms, though some (e.g. cyanobacteria) sometimes aggregate into visible mats or filaments. Among the eukaryotes are unicellular microorganisms often referred to as protists, which include the photosynthetic phytoplankton as well as some heterotrophic organisms (e.g. amoebae). Within this diverse collective of microorganisms, biodegradation of oil compounds is primarily associated with bacterial processes. In the marine environment the archaeal responses to oil pollution have mainly been considered low when compared to bacterial responses (e.g. Röling et al. 2004). However, archaea are important members of communities in petroleum reservoirs and are involved in the mineralization of petroleum hydrocarbons, for instance by methanogenesis under anoxic conditions. Recent studies have also implied the contribution of halophilic archaea to the biodegradation of hydrocarbons in the marine environment (Al-Mailem et al. 2010; Liu et al. 2009). Specific to the Arctic marine environment, essentially nothing is known of the archaeal contributions to oil degradation. 

Among eukaryotes, degradation of oil is mainly associated with fungi (Prince 2005). Only a few studies have been conducted to characterize fungal communities in Arctic marine environments (e.g. Gunde-Cimerman et al. 2003; Butinar et al. 2011). Among the microorganisms, our understanding of the protist contribution to oil biodegradation is also limited. Heterotrophic protists may affect petroleum biodegradation indirectly through their role as bacterial predators. Efficient grazing by protists can maintain the bacterial community in the log-growth phase, resulting in increased metabolic rates and thus increased biodegradation rates (Ballestero and Magdol 2011). 

In summary, most evidence for microbial degradation in the Arctic is connected to bacteria and bacterial communities. Our focus in this section will be on bacterial communities and the bacterial processes involved in oil biodegradation in the Arctic environment. However, the need for greater knowledge related to the contribution of archaeal and protistan organisms to oil biodegradation is an incentive to develop a better understanding of their contribution to oil biodegradation and microbial ecology in the Arctic. 

5.1.1 The Microbiology of the Arctic Oceans Transport routes

The Arctic Ocean represents a complex system of currents with influx and efflux of water (see Figure 5-1).  Cold and relatively less saline water enters the Arctic Ocean through the narrow Bering Strait between Alaska and Siberia, while warmer, more saline surface waters from the Atlantic penetrate the Arctic Ocean and are cooled as they move through the Greenland Sea and the Norwegian Sea. Water reaching the Arctic Ocean basin is swept into a huge circular current — driven by strong winds — the Beaufort Gyre. Siberian and Canadian rivers drain into the circular marine current to create a captured internal reservoir of relatively fresh water. Periodically, the circular current weakens, allowing large volumes of fresh water to leak out and cross the Arctic in the Transpolar Current. The water exits the Arctic Ocean via several “gateways.” It can flow through the Fram Strait, between northeast Greenland and Svalbard Island, and then branch around either side of Iceland. It can flow around the west side of Greenland through Baffin Bay and out Davis Strait. It can also flow through a maze of Canadian islands and out Hudson Strait. These mixes of salty and fresh water also generate Arctic haloclines, a vertical effect in which the cold fresh water lies atop warmer saltier water.

Figure 5-1. Prevailing currents in the Arctic Ocean (Source: Woods Hole Oceanographic Institution;
Figure 5-1. Prevailing currents in the Arctic Ocean (Source: Woods Hole Oceanographic Institution;

The transport routes carry microorganisms into the Arctic from a complex mixture of seawater and river sources, with the North-Atlantic current (number 6 in Figure 5-1) as the single most important influx transport route. This results in cosmopolitanism of microorganisms in the Arctic Ocean and the presence of sometimes unexpected microorganisms in this cold marine environment (Hubert et al. 2009).

Significant to the discussion of currents, water masses, and effects on microbial population structures, a considerable part of the Arctic consists of one- or multi-year ice coverage. Since marine ice is frozen seawater the microbes frozen into the ice are transported with ice movement. This movement essentially follows two routes; the Beaufort Gyre circulating clockwise around the North Pole and the Transpolar Drift Stream, where ice moves from the Siberian coast of Russia across the Arctic basin, exiting into the North Atlantic off the east coast of Greenland (number 5 in Figure 1).  During ice growth, brine pockets are generated in the ice, since ice crystal generation is almost devoid of impurities (Petrich and Eicken 2010).  Brine accumulations are first generated as pockets, and later as chimney-like tubes termed brine channels. Microbes require a fluid environment for active metabolism, and these brine channels represent a fluid microenvironment within the ice mass. These channels therefore become important ecological niches for microbes which are able to survive in the high salinity and subzero temperatures in these systems. Eventually, contact with seawater will result in nutrient transport and reduced salinity in the channels. If channels are wide enough (approximately 2 mm in diameter), they are able to support counter-flow, i.e. simultaneous upward and downward movement inside the same channel (Lake and Lewis 1970).  Despite the potential for flow and mixing with bulk marine water, brine salinity tends to increase with distance to the seawater.   These salinity gradients in brine channels may result in gradients of microbial population density.  In winter, the apparent effect is higher bacterial and algal concentrations in the lower than the upper parts of the ice (Gradinger and Zhang 1997). However, in late spring and summer with rising air temperatures, the opposite situation is observed. The ice is warmed up from the top, becoming more porous, and melt water penetrates the porous ice and generates a linear bulk salinity profile that is commonly observed in the upper 20 to 50 cm of the ice during melt. The organisms in the brine channels are therefore exposed to fluctuating and physiologically challenging salinity conditions during the periods of ice freezing and melting (Faksness et al. 2011). Since much of the brines are drained off the ice during the first year after freezing, multi-year ice tends to have lower salinity and density than first-year ice (Tang et al. 2007), resulting in fewer brine pockets and also fewer possibilities for active microbial metabolism in the ice. Microbial populations in the Arctic Ocean

The population structures of bacteria in Arctic seawater are comparable to those in seawater from temperate regions, with the predominance of Alphaproteobacteria, Flavobacteria/Bacteroidetes,Gammaproteobacteria and Verrucomicrobia constituting more than 90% of the communities (Comeau et al. 2011; Teske et al. 2011; Ghiglione et al. 2012). It is also relevant to compare the microbial communities in the Arctic and Southern Oceans, since the two geographical areas have similar climatic conditions. Although some comparative studies of the microbial communities in Arctic and Antarctic marine environments indicated a high degree of resemblance (e.g. Bano et al. 2004; Brinkmeyer et al. 2003), a recent pole-to-pole study of surface and deep marine bacterial communities revealed significant differences, with 78% of operational taxonomic units (OTUs) unique to the Southern Ocean and 70% unique to the Arctic Ocean. Despite these dissimilarities, polar ocean bacterial communities were more similar to each other than to lower latitude pelagic communities (Ghiglione et al. 2012).

At a more localized scale, sea ice microbial communities may differ from those in the surrounding seawater. A study of first-year Arctic ice showed differences between ice and source seawater populations that were characterized by an increased abundance of Gammaproteobacteria and a lower abundance of Bacteroidetes in sea ice relative to seawater.  Winter sea ice communities were more similar to autumn water communities; species-specific die off processes were not observed in sea ice.  The implication was that winter sea ice communities are stable, whereas seawater communities undergo seasonal succession. The Alphaproteobacteria dominated in both environments (Collins et al. 2010). A study of multi-year ice revealed overall dominance of Gammaproteobacteria, as well as an increase ofBacteroidetes in the sea ice when compared to source seawater; the abundance of Alphaproteobacteria was greatly reduced in sea ice relative to the abundance in surrounding seawater (Bowman et al. 2012). A number of studies have also investigated the microbial communities in Arctic sediments, which may be regarded as pristine environments compared to most other sediments investigated. Studies from an Arctic fjord (Svalbard) showed that the Alphaproteobacteria predominated in the overlying seawater, while Gammaproteobacteria were more abundant in surface sediments. Deeper anoxic sediment layers were dominated by Deltaproteobacteria, which include common genera of strictly anaerobic bacteria associated with marine sediments (Ravenschlag et al. 2001; Teske et al. 2011).

5.1.2 Microbial Adaptation to Arctic Conditions

The primary climatic condition associated with the Arctic is low temperature, and therefore most reviews and fundamental studies of Arctic microbiology focus on low temperature and psychrophilic (cold-loving) microbes. However, other conditions are also specific for this environment, including extreme light/dark conditions in the Arctic summer and winter, respectively. The Arctic area also includes coverage, with 9-12 million km2 of pack ice with average ice thicknesses of 3-4 m, with ridges up to 20 m thick. As described above the microbes in this ice are not only challenged by the subzero temperature, but also by high salt concentrations in the brine channels. Low temperature and microbial adaptions

The temperature of the Arctic Ocean normally does not exceed 4-5°C, with cold (close to 0°C) low-salinity surface water and warmer high-salinity water (up to 5°C) below 50 m depth. The marine organisms in the Arctic are therefore consistently exposed to low temperatures. Numerous studies of microbial adaptions to low temperature have been published (e.g.  Brakstad et al. 2008; Helmke and Weyland, 2004; Knoblauch et al. 1999; Robador et al. 2009). As the temperature decreases with concomitant decrease in the thermal energy of a system (enthalpy), increased stability and rigidity of biomolecules occur. Proteins become less flexible, while the secondary structures of DNA and RNA become more stable, and the processes of DNA replication, transcription of RNA and translation of proteins are inhibited (Bakermans 2012). However, psychrophilic microorganisms have adapted to these low-temperature conditions in a number of ways:

  • Enzymes in bacteria isolated from sea ice may be activated by the cold, with detectable catalytic activity well below the freezing point of seawater (Groudieva et al. 2004). The enzymes of psychrophilic microbes are characterized by increased flexibility of active sites resulting from structural modifications to address freezing temperatures.  These modifications may include less enzyme core hydrophobicity, increased surface polarity and fewer interactions between amino acids (hydrogen bonds, salt and disulphide bridges). These characteristics facilitate retention of enzymatic activities at low temperature (Bakersman 2012).
  • Nucleic acids show adaption to low temperature at the sequence level in psychrophiles, as exemplified by increased uracil content in ribosomal RNA and dihydrouridine content in transfer RNA as a result of decreased temperature (Khachane et al. 2005; Dalluge et al. 1997).
  • Microbial membrane structures may crystallize at low temperatures, impairing function. However, in psychrophiles, membrane fluidity is retained by increasing the proportion of unsaturated fatty acids and by desaturation of membrane lipids, resulting in unsaturated fatty acyl chains and less tightly packed lipid chains (Russel 2008).
  • Microorganisms can be challenged in ice by reduced water availability due to the formation of ice crystals. However, psychrophiles can combat the effects of reduced water activity by the synthesis of compatible solutes such as sugars, amino acids, alcohols or cryoprotective proteins. Ice crystal formation can also be prevented by production of anti-nucleating materials (Bakersman 2012).
  • Psychrophilic bacteria in brine channels are challenged by both low temperature and high salinity.  These may produce extracellular polymeric substances (exopolysaccharides), which have a cryoprotective role in the sea ice brine channels, as well as binding essential cationic trace metals to enhance halotolerance (Nichols et al. 2005).
  • Microbes exposed to large drops in temperature may produce cold shock and cold acclimation proteins (Berger et al. 1996). Cold shock proteins are supposed to be involved in protein translation regulation, while cold acclimation proteins show high catalytic activity at low temperatures and rapid inactivation at moderate temperatures (Fukunaga et al. 1999). Light and microbial phototrophs

In Arctic regions, with a long polar summer and a correspondingly long polar winter and associated widespread ice coverage, phototrophic organisms must tackle a number of challenges.  For example, phytoplankton communities responded rapidly and increased in numbers by an order of magnitude in the Beaufort Sea with the increased solar irradiation in May, despite the presence of sea ice. However, eukaryotic phototrophs somehow also persisted throughout the winter darkness (Terrado et al. 2008). Among phototrophic bacteria isolated from the Arctic Ocean were photoheterotrophic microbes, which are capable of both utilizing dissolved organic materials and harvesting light energy.  Photoheterotrophic taxa included coccoid cyanobacteria (Synechococcus and Prochlorococcus), aerobic anoxygenic phototrophic (AAP) bacteria, and proteorhodopsin (PR)-containing bacteria. In a study of photoheterotrophic microbes in the Arctic Ocean in the summer and winter it was observed that some of these bacteria (AAP and PR containing bacteria) decreased from summer to winter, in parallel with a threefold decrease in the total prokaryotic community, while the abundance of Synechococcus did not decrease in winter (Cottrell and Kirchman 2009). These data demonstrated the ability of phototrophs to switch from photosynthesis to heterotrophic activities during the winter.  Characterization of green light-absorbing PR from bacterial isolates from the Arctic Ocean showed a slower photocycle, relatively larger change in activation energy of the transition between the oxygen intermediate and the ground state compared to PR from bacterial phototrophs isolated from temperate seawater (Jung et al. 2008).

Photosynthesizing microbes have also been observed within sea ice. Marine algae seem to be more sensitive to brine salinity than bacteria and therefore are detected mainly in the lower parts of sea ice (lower salinity in winter associated with contact with seawater; Gradinger and Zhang 1997). Recent studies have also identified marine autotrophic bacteria in marine ice indicating the potential ability for ongoing use of dissolved organic materials (Díez et al. 2012). Marine ice and microbial survival and metabolism

Conditions in marine ice vary considerably from those in seawater. The temperature is lower in the ice relative to fluid water, and may drop as low as the air temperature during the polar winter. Transmission of light through the ice is severely reduced compared to seawater, and light may be entirely absent when the ice is covered by a snow cap. In first-year ice, brine inclusion networks are generated by salting-out processes, as described in previous sections. The brine channels of the ice provide liquid saline niches at subzero temperatures which enable microbial motility and metabolic activity (Junge et al. 2002; 2003; 2004; 2006). The brine channels also act as a matrix for transport of soluble organic matter and other nutrients.  In the brine channels the ice temperatures can be as low as -20°C and salinity conditions can be as high as 200 Practical Salinity Units (Salinity in normal seawater is 35 PSU). Though challenging to microbial life, laboratory experiments have shown that bacteria (Colwellia psychroerythraea) were able to incorporate amino acids into proteins at temperatures as low as -20°C in brines (Junge et al. 2006). This metabolic activity was associated with particles or with the surfaces of the brine channels (Junge et al. 2003; 2004). In addition, the ability to grow at subzero temperatures has been demonstrated in the bacterium Psychromonas ingrahamii, which was cultured at temperatures as low as ‑12°C (Breezee et al. 2004). The brine channels may become depleted in oxygen, for instance if microbial processes occur without oxygen renewal (seawater or photosynthesis), and anaerobic denitrification processes have been measured in marine ice (Rysgaard and Glud 2004). These studies therefore demonstrate that bacterial activity can take place in marine ice, both with respect to motility within the ice and active metabolism. Recently, Mykytzuk et al. (2013) presented a detailed characterization of the physiological adaptations that enable a halotolerant psychrophilic permafrost bacterium to grow and metabolize at temperatures as low as -15°C.  The implication is that halotolerant psychrophilic species may also exist in the ice.