African Journal of
Microbiology Research

  • Abbreviation: Afr. J. Microbiol. Res.
  • Language: English
  • ISSN: 1996-0808
  • DOI: 10.5897/AJMR
  • Start Year: 2007
  • Published Articles: 5238

Review

Response of microbial communities to oil spill in the Gulf of Mexico: A review

Linda Adzigbli
  • Linda Adzigbli
  • Pearl Research Institute, Guangdong Ocean University, Zhanjiang 524025, China.
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Hernado P. Bacosa
  • Hernado P. Bacosa
  • College of Science and Environment, Mindanao State University at Naawan, Misamis Oriental 9023, Philippines.
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Yuewen Deng
  • Yuewen Deng
  • Pearl Research Institute, Guangdong Ocean University, Zhanjiang 524025, China.
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  •  Received: 14 March 2018
  •  Accepted: 08 June 2018
  •  Published: 21 June 2018

 ABSTRACT

Crude oil has become a part of the marine ecosystem through natural seeps and oil spills. Microbial communities have adopted various response mechanisms to adjust to oil spills that contaminate the marine environment and help restore the ecosystem to its original state. These response mechanisms ranges from change in indigenous microbial community composition, change in microbial diversity to gene diversity and modification. An instance for review was the deep-water horizon (DWH) oil spill in the Gulf of Mexico. The DWH oil spill was distinctive from other spills in terms of profundity, extent as well as its scale hence fears and enquiries about the state and outcome of the hydrocarbons at large is required. The main inquiry was about the metabolism ability of microbial communities; the ways, and to what degree the hydrocarbons can be metabolized. Various researches after the spill revealed that change in the successional patterns from the water column, shallow water and bottomless sea sediments to the coastline sediments saw the dominance of Roseobacter cluster within the Alphaproteobacteria on the surface, the Deltaproteobacteria closest to the wellhead, Cycloclasticus in shallow oil slicks, Colwellia and Alteromonas in the deep-sea hydrocarbon plume and sediment. These microbial communities help in bioremediation of oil during oil spills through their response mechanism. Factors such as nutrient limitation, hydrocarbon availability, ocean mixing and circulation among others also limit the rate at which microbial communities degrade hydrocarbons. This review outlines the response mechanism of microorganisms and how they help in hydrocarbon degradation.

Key words: Oil spills, microbial communities, microbial response, microbial degradation, hydrocarbons, deepwater horizon, Gulf of Mexico.


 INTRODUCTION

Crude oil has become a vital part of the world’s economy and industrial growth and is currently in a period of industrial development, alteration and increase (Bao et al., 2014). An increase in this industry involved in production, transportation and storage of oil has exposed most shores along oil mining areas and marine environment to oil spill accident (McGenity et al., 2012) from cargo/wholesale ocean carriers which are the major source carriers of oil (Bao et al., 2014). These oil spills affect human life, the environment and ecosystem as a whole. For example, the 2002 Prestige oil spill affected shores of Spain with about 66% of species abundance lost (Huz et al., 2005); the Deepwater Horizon spill (2010) conceded biodiversity of vertebrates and metazoan meiofauna (Baguley et al., 2015). Some other intense oil spill examples are the tanker collision in the Mumbai coast and the oil spill in Montora (Sakthipriya et al., 2015)
 
Microbial communities are known to control most major processes that occur in the marine environment (Karl, 2007). One important function and process is biodegradation of contaminants and nutrient recycling that helps to ensure an effective and efficient ecosystem (Wu et al., 2014). Hydrocarbon degradation by microorganisms has received much consideration because of its un- hazardous, inflammability, extensive and environmentally friendly state when likened to other orthodox methods (Sakthipriya et al., 2015). Microorganism from all the three domains of life are known to utilize the ~600 000 tons of oil which moves into the marine ecosystem from natural leaks yearly (NRC, 2003). A total of 175 prokaryotic genera of microorganisms from seven phyla of Bacteria, Archaea, and an equivalent amount of fungal genera, can utilize hydrocarbons as the only or main source of carbon (Hazen et al., 2015). Most of these microorganisms are found in the water column, sea bed sediments and on the shorelines of the marine environment through the tropics to the Polar Regions eg. Alphaproteobacteria, Gammaproteobacteria, Deltaproteobacteria, Pelagibacter, Actinobacteria, Planctomycetes and Bacteroidetes (Yang et al., 2016).
 
Upon the introduction of crude oil in the oceanic ecosystem, there is a change in microbial community consisting of numerous mutually surviving species which is described via resource sharing (Yakimov et al., 2005). The native oil utilizing bacteria becomes enriched, with organisms of the order Oceanospirillales comprising up to 90% of bacterial community, when related with 5% of the pure sample (Hazen et al., 2015). McNutt et al. (2012) after the DWH oil spill in the Gulf of Mexico projected ~5.0 M drums to ∼210 M tons of oil and gas released. Other research from these oil spill in April 2010 discovered impacts of the oil on marine organisms populations involving corals (Goodbody-Gringley et al., 2013), meio-, macro- and mega-fauna (Fisher et al., 2014) coupled with its influence on microorganisms assemblies (Hazen et al., 2010; Edwards et al., 2011; Mason et al., 2012; Redmond and Valentine, 2012; Gutierrez et al., 2013).
 
This study reviews the responses of microbial communities from the introduction of oil from oil spills to the marine environment, from the water column, shallow water, and bottomless sea sediments to the coastline sediments, in particular, with reference to the Deepwater Horizon oil spill.

 


 CONSTITUENTS OF CRUDE OIL AND BIODEGRADATION

Crude oil is a composite combination of organic compounds principally consisting of hydrocarbons (HC), averagely ∼30% linear and branched alkanes, ~30% cyclic alkanes, ~30% aromatics  and ~10% molecules with heteroatoms such as sulphur, oxygen and nitrogen (Tissot and Welte, 1984) with the latter giving oils most of their color. The aromatics consist of molecules that contain at least one single or condensed rings and aromatic ring, coupled by recurring and linear alkane substituents like the monocyclic (Tissot and Welte, 1984). The aromatics also comprise of polycyclic aromatic hydrocarbons (PAHs). Low molecular weight compounds (benzene, naphthalene and anthracene) are favorably degraded and high molecular weight (pyrene and fluoranthenes) being also broken down (Bacosa and Inoue, 2015). The polar fractions of crude oil comprise mainly of Asphaltenes and resins; however, the characterization of this polar molecule has not yet been widely done in the marine ecosystem. Microbes are able to take up some, and others if constantly exposed to the sun are generated by photochemistry (Aeppli et al., 2012), making their gross fate in the environment unclear. Hydrocarbons with about 40 carbon atoms are near total biodegradability in a one or two months when presented with a conducive atmosphere, except for certain hopanes and steranes (Prince et al., 2013); however bigger molecules degrade much more slowly, example are the constituents intended for roads.  
 
The introduction of oil into a marine ecosystem makes considerable excess of carbon available in the development of microorganisms (Prince et al., 2003). However, unavailability of nutrients (nitrogen and phosphorus) is able to lessen the development of microbes and hence oil degradation (Liu et al., 2017). In an attempt to promote oil degradation on diverse coastlines (including the Arctic), fertilizers containing available nitrogen and phosphorus were added (Prince et al., 2003). Wide research and field-testing discovered that the development of hydrocarbon degrading micro- organisms was stimulated by adding nutrients and consequently raises the detected speed of oil decomposition (Atlas and Bragg, 2009).
 
 
 
 
Microbial degradation eliminates the hydrocarbons in marine environs and regenerates the oil polluted biota (Al-Hadhrami, 1995). Significant progress has been made within previous era in understanding hydrocarbons degradation by microorganisms (Atlas et al., 2011). The major microbes that help in degradation of oil have been identified from the 3 domains of life: bacteria, archaea and eukaryotes (Bacosa et al., 2015a) via different degradation pathways (Table 1). Most of the active oil degrading microbes are bacteria and over 79 genera of bacteria have been known to be able to use hydrocarbons as  the main and exclusive origin of energy among those with the ability to breakdown or convert hydrocarbons (Head et al., 2006). The oceanic ecosystem only shelters a minimal of 25 genera of bacteria that decompose hydrocarbons and are known primarily for pollutants attenuation (Das and Chandran, 2011). Due to the diversified nature of hydrocarbon compounds related to oil (iso-, cyclo, and linear alkanes, monoaromatic compounds and polycyclic aromatic hydrocarbons), the breakdown of different groups of hydrocarbon compounds needs different microorganisms with distinct biochemical mechanisms (Timmis et al., 2010). Distinctively, microbial communities have the ability to biologically breakdown a large array of hydrocarbons collectively as compared to an individual microorganism. Succeeding the DWH spill, there was a fast improvement in the quantity of hydrocarbon- degrading microorganisms in the water column, shallow and subsurface column water and ruled by recognized hydrocarbon-decomposing bacteria (King et al., 2015).
 
 
The degradation of hydrocarbons by microorganisms mostly involves oxygen combined with hydrocarbons to produce water and carbon dioxide achieved by the enzymes oxygenase and peroxidase (Figure 1). Hence, free oxygen is required for degradation to occur through these pathways. Shallow waters hardly lack oxygen; however, the concentration of oxygen can reduce as it travels through the water column and sometimes lacking in bottom waters. Most often, sediments usually lack oxygen (anoxic condition) below the surface; however, in some cases, oxygen is able to infiltrate below to the seabed (Roy et al., 2012). It is unlikely for anoxic condition on shallow slicks of the water plume to prevent or reduce biodegradation due to the ability of oil droplets to dilute quickly. Anoxic conditions can however occur in lower levels or bottom depths depending on the oil concentration and degree of oxygen renewal by waves and currents. The degradation of hydrocarbons by microorganisms via aerobic pathways (Figure 2) is known as aerobic biodegradation of hydrocarbons. The Gammaproteobacteria, Alphaproteobacteria and Betaproteobacteria are the major oil-degrading bacteria that utilize oxygen and are mostly outlined (Head et al., 2006; Van Beilen and Funhoff, 2007).
 
 
 
Biodegradation by aerobic microorganisms is activated by monooxygenase and dioxygenase enzymes (Austin and Callaghan, 2013). Alcanivorax borkumensis an oil-degrading microorganism and a marine gammaproteobacterium is widely studied and defined to consume wide array of aliphatic hydrocarbons (Dos Santos et al., 2010) through various pathways using terminal oxidation process through numerous enzymes (Table 2) introducing hydroxyl groups to the organic compounds (alkB1, P450 and cytochrome monooxygenase) (Sabirova et al., 2006).
 
 
Despite the fact that hydrocarbon degradation by aerobes symbolizes a fast and acknowledged method (Fritsche  and  Hofrichter, 2008), much consideration is given to degradation by anaerobes (Heider and Schühle, 2013) for its role in marine ecosystems associated with oil spills (Head et al., 2006).
 
The scale of anaerobic hydrocarbon degradation is slow as compared to aerobic hydrocarbon degradation; however, it is mostly needed in marine sediments (Roy et al., 2012). When oxygen is limiting, Fe3+, SO42− and NO3− are known to occur for biodegradation of hydrocarbon (Foght, 2008). Marine harbor sediments are known to degrade petroleum hydrocarbons when oxygen is limiting and sulfate and iron-reducing conditions are present (Coates et al., 1996). For example, the Caspian Sea permanently lacks oxygen in bottom waters, so it is possible that any hydrocarbon degradation is under oxygen limitation. Microorganisms adapted to oxygen limiting conditions comprises of sulfate reducers, denitrifying and nitrate ammonifying bacteria, phototrophs, and metal ion reducers, with the ability of breaking down several hydrocarbons, ranging from n-alkanes and n-alkenes to the more stubborn aromatic compounds (Heider and Schühle, 2013).
 
The often discussed method for initiating and breakdown of hydrocarbon under anaerobic conditions is the addition of fumarate (Heider and Schühle, 2013). Other substitute methods defined include intra-aerobic hydroxylation, oxygen-independent hydroxylation and carboxylation (Callaghan, 2013a; Heider and Schühle, 2013) (Figure 2).
 
Activation for further metabolism in aerobic pathway requires terminal and sub-terminal reaction for aliphatic HCs and peripherical hydroxylation reactions for aromatic HCs. Anaerobic pathways require double reaction for this process (Garcia and Oliveira, 2013).
 

 


 POST SPILL MICROBIAL RESPONSE MECHANISMS

Research over time has proven that after an oil spill incident, microbial communities mostly make use of 3 major response mechanism from the water column, surface water and bottomless sea sediments to the shoreline sediments mainly change in succession of native microbial community structure, change in microbial diversity and gene diversity and modification (Engel and Gupta, 2014; Rodriguezr et al., 2015).
 
For instance, with respect to DWH oil spill, discharge was a Louisiana lighter crude oil (contains little sulfur and great gasoline/kerosene fractions as compared to denser oils); dominated by alkanes (saturated hydrocarbons), 16% aromatic hydrocarbons and 10% polar compounds (Reddy et al., 2012). Shortly succeeding the blast, shallow waters were covered with huge quantities of oil. However assumptions were undiscovered but then possibly bulky quantities of oil was confined in deep waters due to the great depth. In the first month of the DWH accident, a bottomless water oil column interrelated with dispersed MC252 oil was discovered at ∼1100 m depth (Hazen et al., 2010). The column was composed of a composite combination of hydrocarbons comprising of alkanes, monoaromatic hydrocarbons (BTEX) and polycyclic aromatic hydrocarbons (PAHs) with concentrations up to189 μg/L (ppb) and extending principally in a west-south west direction from the still gushing wellhead (Reddy et al., 2012). These hydrocarbons are more often than not differentiated by known biomarkers and their corresponding fractions. Additionally, constituents of natural gas; methane, ethane and propane too was discovered at significant, then again doubtful levels (Joye et al., 2011; Reddy et al., 2012). This composite combination of hydrocarbons discharged at bottomless waters and in cold waters (4 to 6°C) lead to microbial biomass bloom in the column (Hazen et al., 2010).
 
In the water column, it was noticed that there was a substantial difference and variety deficit in deep and shallow oil slick populations when compared with populations at the non-oil impacted water column. This was due to the phylogenetic shift undergone by the indigenous populations (Redmond and Valentine, 2012; Yang et al., 2016). Findings according to Liu et al. (2017) stated the role of environmental factors especially temperature on microbial succession and shift. Further discoveries stated that succession patterns at every specific location were determined by the availability of specific hydrocarbon compounds (Dubinsky et al., 2013). The carbon branded hydrocarbons and segregation methods gave extra proof of fluctuating populations of impacted water column with ability of disintegrating several groups of hydrocarbons (Gutierrez et al., 2013). The 16S rRNA studies of microorganisms sample within the first and second month after the DWH spill saw the dominance of an uncultivated gammaproteobacterium from order Oceanospirillales dominating (Hazen et al., 2010; Redmond and Valentine, 2012; Mason et al., 2012). Even though GeoChip 4.0 submitted proof of enriched genes included in aerobic and anaerobic hydrocarbon degradation in the column, metatranscriptomic data obtained from the same cruise samples suggested aerobic degradation of hydrocarbons as most dominant on site procedure during that time (Mason et al., 2012). Genes that help in aerobic alkane degradation (e.g., alkane monooxygenase, cyclohexanol dehydrogenase and cyclohexanone monooxygenase) remained highly at significant peaks in the column metatranscriptomes. These genes were also found in single-cell genomes of Oceanospirillales, however aromatic hydrocarbon degradation were discovered in low levels or remained undiscovered (Mason et al., 2012). Around mid- to late June 2010, there was change in succession of microbial community in the water column, dominantly by two different gammaproteobacteria groups, Cycloclasticus and Colwellia (Redmond and Valentine, 2012). With regards to microcosm experiments, the crude oil enriched areas (methane, ethane, propane and benzene) were dominated by Colwellia spp., hence the anticipation of its essential role of degrading ethane and propane in situ within this period (Redmond and Valentine, 2012). Transcriptomic data further revealed that the Colwellia spp. was active and succeeded preceding Oceanospirillales because of their gaseous and aromatic hydrocarbon degradation ability (Mason et al., 2014a). The Colwellia spp. experienced a bloom in June 2010 even though they were scarce in the column during late May 2010 (Mason et al., 2012). By September 2010, initially discovered microorganisms (Oceanospirillales Cycloclasticus and Colwellia) were substituted by initially undiscovered methylotrophic bacteria (Methylococcaceae, Methylophaga and Methylophilaceae), Flavobacteria and Rhodobacterales due to the presence of  methane and methane oxidation observed in minute quantities in the September plume, in addition to the enrichments achieved by the September plume samples (Redmond and Valentine, 2012). Later in October 2010 and July 2011, the analysis of microbial community composition (clone libraries and pyrosequencing) from post-column samples showed likeness for the pre-spill pelagic community (800 m, March 2010) (Yang et al., 2016).
 
The surface water of the Gulf of Mexico in May 2010 showed dominating population of gammaproteobacteria and cycloclasticus (known to degrade aromatic hydrocarbons), similar to that of the deep water plume (Yang et al., 2016). However, pyrosequencing of oil mousses and clone library studies from other distinct sites within this same period showed a dominance (above 65%) of alpha and gammaproteobacteria and cyanobacteria (Redmond and Valentine, 2012), hence highlighting the distinction of surface slick communities from the bottomless water column. There is a possibility for both shallow slick and bottomless water column undergoing the same succession changes of microbial community composition dependent on type and availability of hydrocarbons at each definite time and location.
 
The deep-sea sediments are a home of various microbial communities (Bacosa et al., 2018, 2015b) similar in genera with the water column. After the DWH spill, large quantity of PAH compounds (>24,000 µg/kg) were observed in deep-sea sediments near the oil platform as compared to distant cores (∼50 µg/kg); hence, the uncovering of the indigenous microflora to aromatic hydrocarbons near the oil platform (OSAT-I, 2010). Metagenomic analysis and targeted functional gene assays of subsurface (1.5 to 3 cm) deep sea sediment cores from September to October 2010 was highly dominated by Deltaproteobacteria and anaerobic degrading genes for aliphatic and aromatic hydrocarbons (For example, bssA, benzoyl-CoA reductase genes and assA) in the sediments located near the well (1-3 km) in espect to the distant (128 km) control samples (Kimes et al., 2013). Alphaproteobacteria was second-most abundant and was  in  line  with  alphaproteobacterial blooms observed in metagenomic analyses of seafloor sediments collected in September 2010 (Mason et al., 2014). Other discovered groups according to Yang et al. (2016) are the Deltaproteobacteria, Bacteroidetes, Actinobacteria, Planctomycetes and Verrucomicrobia. The abundance of the groups increased or decreased over time depending on specific hydrocarbon availability and successional changes of microbial communities observed at the order, family or genus level of the various groups (Figure 3). The presence of Oceanospirillales, even though in low quantities with no variation at contaminated and non-contaminated sites, presented the genomic proof of aerobic hydrocarbon-degradation in sediments (Kimes et al., 2013).
 
 
Metagenomic analysis of samples taken 3 years after the spill (June 2013) still revealed genes related to the initial oxidation of aromatic rings, alkane monooxygenase and those involved in metabolizing hydrocarbon degradation by-products (alcohol and cyclohexanol dehydrogenases), and fatty acid metabolism was the most abundant (Bacosa et al. In Press). Bacterial communities of Alteromonadales, Oceanospirillales, Methylococcales, Rhodobacterales and Bdellovibrionales increased in oil treatments.
 
In coastal sediments/sands, oils discovered after an oil spill were extensively weathered; mostly reducing C9-C16 n-alkanes (0.3 to 1.6% of total composition as compared to 54% in MC252 oil) and BTEX/C3-benzenes (an order of magnitude lower levels) (Liu et al., 2012). The concentrations of PAH are also altered losing the dominant MC252 PAH and naphthalene, reduced to 3-9% of total PAHs in relation to 64% in unaltered MC252 oil. However, according to Engel and Gupta (2014), coastal sandy beach had shifting regime of microbial communities with respect to depth, location and time. Some of the dominant groups found on the open beach and swash zones were Gammaproteobacteria, Alphaproteobacteria, Firmicutes, Bacteroidetes, Enterobacteriales, Xanthomonadales and Chromatiales. Successional changes occurred in the various species of these groups over time. Aeppli et al. (2012) discovered high levels (10 times less in MC252) of oxyhydrocarbons (major component of tar balls) in beach sand after a long term study (18 months after spill). Kiruri et al. (2013) discovered obstinate free radicals on coastal beach Tar balls providing evidence of the oxidation of aromatic hydrocarbons with transition metals and weathering of hydrocarbon through multiple processes. However, it should be noted that these processes vary based on the site deposited.
 
FACTORS AFFECTING MICROBIAL BIODEGRADATION
 
Microbial degradation of oil spills is a composite procedure influenced by several features of the oil and the surroundings. For example,  the  scope of oil droplets dissemination determines the prospects of the oil in the subsequent time frame (Yapa et al., 2012). Physical and microbial processes degrade tiny oil droplets easily (Hazen et al., 2015).
 
Dubinsky et al. (2013) established that the simultaneous operation of multiple hydrocarbon-degrading bacteria throughout the spill was regulated by change of hydrocarbon availability. For example, Oceanospirillales and Pseudomonas were the major genera in the initial stages of the oil spill with very high n-alkanes and cycloalkanes levels. Kleindienst et al. (2015) observed a change in deep plume community with respect to a change in quantity of hydrocarbon available (increased aromatic hydrocarbons and decreased petroleum hydrocarbons), that is, Colwellia, Cycloclasticus and Pseudoalteromonas dominating.
 
The process of biodegradation also involves degrading transformational byproducts and exopolymeric substances yielded by microbial communities to combine hydro- carbons and enable oil availability. The measurement of a higher peptidase activity and enzymatic hydrolysis of carbohydrates in the water samples within the oil spill plume when likened to the outside predicted that, the deep-water column microbial communities were structured to degrade singled out array of explicit high molecular weight substrates (Ziervogel and Arnosti, 2014). Gutierrez et al. (2013) researched on the function of amphiphilic exopolysaccharides produced by indigenous Halomonas bacteria for the period of the DWH oil spill. They discovered that strain TG39 produced Halomonas exopolysaccharides which efficiently amplified the solubility of aromatic hydrocarbons and improved their degradation, hence influencing oil removal and oil aggregates formation.
 
Nutrient deficiency is a normal limiting factor for microbial growth. Nitrogen and phosphorous are known as the key restrictive elements for oil degradation in the sea (Beyer et al., 2016). In oil-contaminated shallow waters of the Northern Gulf of Mexico (NGOM), it has been proposed that deficiency of dissolved nutrients mainly phosphate, reduces microbial growth (Liu et al., 2017). This is because when incubation mixtures were altered with nutrients, bacterial cell numbers and biomass improved speedily (Edwards et al., 2011). The addition of nitrogen fertilizers mainly on shorelines and uric acid at sea help stimulate and enhance oil bioremediation (Ron and Rosenberg, 2014).
 
Oceanic mixing and circulation processes are essential for microbial oil degradation (Beyer et al., 2016). The assessment of the impact of physical mixing processes on marine bacterial communities showcased biodegradation patterns of a faster growth rate for bacteria from seed populations that are scarce in nature. There is possibility of major participation of oceanic mixing process in allocating hydrocarbons, accompanied by bacterial blooms, and accelerated hydrocarbon degradation across an autoinoculation effect inside the northeast Gulf waters. The impacts of mixing and circulation processes on degradation of oil spills was shown by the higher abundance of HC-degrading bacteria in past bloomed waters that later re-circulated to the spill site, feeding successive bacterial blooms (Valentine et al., 2012).
 

 


 CONCLUSION

In an era where crude oil production and consumption is on the rise, oil spills are inevitable in the marine environment. Even though the frequency and quantity of oil spills have reduced over the years, the marine environment still remains a reservoir for oil from natural seeps. Microbial communities have developed the ability to degrade these crude oil products. Bacteria from the phylum Proteobacteria has been known as the major crude oil degrading microbe. Other microbial groups: Firmicutes, Bacteroidetes and some arhaeal groups also have the ability to breakdown hydrocarbons. They have developed mechanisms such as acquisition of oil degrading functional genes, change in biodiversity where species with the ability to degrade specific hydrocarbons dominate and change in succession patterns. How microbial communities respond to crude oil has been far researched over the years; however, the amount and quantity of hydrocarbons degraded is still lacking. Other researches have also focused on the large fractions of oil introduced into the system leaving the residues, weathered components and the biodegraded byproducts which have detrimental effects on other marine organisms. More researches should focus on the concentration and quantity of hydrocarbons degraded by specific oil degrading microbial species and using oil residues from past spills to assess the impacts and possible ways for total ecosystem recovery.


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.

 



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