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Note added. Microbial Oil-Degrading Populations in Cold Water Environments

In the aftermath of the Deepwater Horizon incident, a large body of new information has been collected and integrated with our already existing understanding of the microbial response to oil spilled in the marine environment (Hazen et al. 2010; Mason et al. 2012; Valentine et al. 2012). In general, in situ sampling and analysis revealed unexpectedly rapid disappearance of released oil in the Gulf of Mexico environment, which is characterized by a temperate climate (Hazen et al. 2010). This rapid disappearance was affected by the prevalence of water-soluble constituents in the crude oil (Reddy et al. 2012), injection of subsea dispersant into the erupting oil flow (Kujawinski et al. 2011), and presence of indigenous oil-degrading microorganisms in this area that is well known for natural seeps of crude oil from reservoirs (Lu et al. 2012). Such indigenous oil-degrading microorganisms are the topic of this section.

Following the Deepwater Horizon incident, extensive analysis of microbial responses was done both in situ and in laboratory microcosms. These analyses support, in general, a paradigm of successive blooms of taxonomically distinct indigenous microbial populations as the oil weathers and labile components are sequentially degraded leaving less-readily degraded components to feed subsequent blooms (Hazen et al. 2010; Valentine et al. 2010; Kostka et al. 2011; Baelum et al. 2012; Beazley et al. 2012; Lu et al. 2012; Mason et al. 2012; Valentine et al. 2012).

Conditions are very different in high latitude marine environments.  As described in previous sections, the Arctic and Antarctic marine environments are characterized by seasonal extremes of photoperiod, spatial variability in salinity and temperature, as well as generally colder surface temperatures compared to the temperate latitudes. These differences may result in different expectations about the rate of oil degradation, as described in previous sections.  They also result in different expectations about the indigenous populations of oil degrading microorganisms.

As mentioned in previous sections, microbial responses to oil in marine environments generally are dominated by bacteria rather than archaea (Roling et al. 2004). Although fungi are known to degrade petroleum compounds in some marine settings (Zinjarde and Pant 2002), few surveys of fungal abundance in high latitude marine environments have been done (Butinar et al. 2011) and thus far none have addressed oil degradation by fungi in high latitude environments. For these reasons, this section focuses on the bacterial component of the marine microbiological community. Indigenous Microorganism Populations

Among the bacterial taxa catalogued in high latitude marine environments, many appear to be specific to that environment (Ghiglione et al. 2012; Sul et al. 2013).  This apparent specificity may be due to truly unique populations, or it may be a function of the limit of detection.  Community members that thrive in the high latitude marine environment grow to relatively high cell densities and are therefore more easily detected.  Various investigations have found that microbial species richness curves are not saturated with typical levels of effort.  This finding has led to the hypothesis that there is an under sampled “rare biosphere” of organisms with low population density (Sogin et al. 2006) that, despite low population levels, can respond to changes in environment and energy source.  This phenomenon may be typified by the explosion of Oceanospiralles and Colwellia populations in the presence of different partitions of spilled oil during the Deepwater Horizon incident (Hazen et al. 2010; Bælum et al. 2012).

Marine ice represents an extreme biosphere with below-zero-centigrade temperatures and high salt concentrations. It has been demonstrated by field studies that bacterial populations in Arctic marine ice are affected by oil pollution, stimulating species of a few genera like Colwellia, Marinomonas and Glaciecola (Brakstad et al. 2008). 

Not all of the microorganisms found in the Arctic oceans are adapted to that environment.  The various currents carry viable microorganisms from diverse locations to the Arctic (Rosnes et al. 1991; Hubert et al. 2009; Hubert et al. 2010); thus, there is an expectation of cosmopolitanism among the free-living microorganisms.  This is not to say that the population structure is homogenous as if the Arctic were a giant mixing bowl.  In fact, there is documented variability in population structures, with different communities associated with water masses of different origins (Galand et al. 2010; Sul et al. 2013).   The presence of non-adapted microorganisms such as thermophiles does, however, indicate that microbial populations adapted to the consumption of natural or human-induced oil releases might be transported to and be present in areas that are not commonly exposed to oil. Population Effects on Oil Degradation

Crude mineral oil is degradable by indigenous microorganism populations in the Arctic marine environment, even at near-freezing temperatures (Brakstad and Bonaunet 2006), although at slower rates compared to higher temperatures (Margesin et al. 2003; Michaud et al. 2004).  Nevertheless, over a time course on the order of weeks substantial biodegradation can be observed in nutrient-enriched cold Arctic seawater (Brakstad and Bonaunet 2006). Community analysis of oil-degrading Arctic microbial consortia indicated that several taxa of bacteria are involved in biodegradation in this environment, including genera related to Pseudoalteromonas, Pseudomonas, Shewanella, Marinobacter, Psychrobacter, and Agreia (Deppe et al. 2005).  Of interest, these are different organisms from those directly associated with degradation in the Deepwater Horizon spill in the Gulf of Mexico, specifically bacteria of the orders Oceanospiralles (Hazen et al. 2010; Kostka et al. 2011) and Alteromonadales (Bælum et al. 2012), among others.

Linear alkanes often are characterized as an easily accessible carbon source, either through degradation or direct incorporation into microbial biomass, in the marine environment (Harayama et al. 1999).  The metabolic pathways for linear, branched, and cyclic alkanes have been studied and described since the 1960s (Jobson et al. 1972, Coates et al. 1997, Feng et al. 2007, Rojo 2009, Gray et al. 2011).  Preferential degradation of short-chain alkanes (represented by C15) over long-chain alkanes (represented by C26) was observed in situ in a deep plume (circa 1,400 m) in the Gulf of Mexico under aerobic conditions (Hazen et al. 2010).  Furthermore, during weathering in subsurface petroleum reservoirs, alkyl chains on substituted soluble PAHs such as alkane-substituted naphthalenes may be transformed even more rapidly than linear alkanes (Jones et al. 2008).  Whether this phenomenon, observed in anaerobic subsurface reservoirs, would occur in the presence of petroleum hydrocarbons released into the deep sea, remains unknown. 

The specific bacteria known to accomplish alkane degradation are numerous (Whyte et al. 1997; Rabus et al. 1999, Hara et al. 2003, van Beilen et al. 2004, Throne-Holst et al. 2006, Feng et al. 2007, Throne-Holst et al. 2007, Wentzel et al. 2007, Rojo 2009, Teramoto et al. 2009, Wasmund et al. 2009, Tapilatu et al. 2010, Alonso-Gutierrez et al. 2011, Teramoto et al. 2011).  Among these, many were characterized from high-latitude marine environments.  Specifically, the Pseudomonas strains isolated by Whyte et al. (1997) from Arctic soils may be transported to the marine environment via runoff.  Alcanivorax species are known to be widespread in marine environments exposed to oil (Hara et al. 2003, van Beilen et al. 2004) and, if not prevalent in the Arctic environment, might be expected to be present because of currents.  Thus, bacteria capable of alkane degradation are expected to be present in the Arctic oceans.

The ability to degrade aromatic hydrocarbons and, in particular, polynuclear aromatic hydrocarbons typically is considered to be less widespread than the ability to degrade alkanes.  For example, some organisms have diverse pathways that confer the ability to degrade polynuclear aromatic hydrocarbons, e.g., Mycobacterium vanbaalenii (Kweon et al. 2011) and various Pseudomonas spp. (Whyte et al.1997). The distribution of these genes among bacteria in Arctic marine environments remains unknown.