Role of microbes in oil spills remediation and degradation of hydrocarbons

Oil spills have become a common sight in the oceans around the world. Such events are the direct result of human error during the transport of crude oil or refined petroleum products across countries. Remediation of oil spills have become an important point of focus for countries and environment agencies across the world. This is due to their increasing apparent harm on environment and wildlife. Oil leakage can also happen through natural processes like petroleum seeps besides coastal facility, fuel freighters and offshore production or extraction wells (1).

Major oil spill events

During an oil spill, massive quantities of liquid hydrocarbons are accidentally released into the environment. Due to oil spills there is wide spread and long term pollution and it disrupts the local ecosystem. Between 1970 and 2015, approximately 5.72 million tonnes of crude oil spilled in the oceans as a result of tanker incidents alone. While in 2015, around 7,000 tonnes was lost to the environment through tankers, pipelines, etc. (2). Although the most memorable oil spill incident in the recent human history was Exxon Valdez, which released 11 million gallons of crude oil. However, it is nowhere near the biggest oil spill in history. The Gulf War Oil spill of 1991, where Iraqi forces released 380-250 million gallons into the Persian Gulf deliberately. Thereby showing the extent of damage in the environment (3).

Impact of oil spills on microbial communities

Soon after an oil spill, a layer of oil floats on the sea surface, where large populations of marine organisms like sea algae, marine mammals, birds and fishes die off, due to poisoning and suffocation. While dispersed oil droplets sink to bottom of the ocean and harm the benthic community. Another major consequence of oil spills is the rapid changes in the local microbial communities. This is due to the sudden availability of large quantity of hydrocarbons which they use as a source of energy and carbon. This microbial degradation of oil hydrocarbons is the main source of oil spills remediation in the natural environment. This has also been used to artificially stimulate remediation in events of extensive spills. Although bacteria, yeast and fungi, all are capable of degrading a complex mixture of oil-hydrocarbons, bacteria possess the highest efficiency. So bacteria are the main degraders of oil hydrocarbons.

Following such oil spill incidents, the local marine microbial community experiences changes in structure and ecology. In such events, microbes capable of utilizing different hydrocarbon compounds as source of energy become the dominant species of that community and consequently assist in biodegradation processes. Post the Exxon Valdez and Deepwater Horizon spills in the Gulf of Mexico, numerous research studies have been undertaken to observe the type and rate of changes within the local microbial communities. These studies reveals multiple factors of community interactions, genetic and metabolic diversity and chemical and geological processes, besides previous pollution history (4).

Types of hydrocarbon degraders

Through chemical, culture-based and metagenomics studies, several species of bacteria and archaea have been shown to possess hydrocarbon degrading capabilities, as shown in the Table below. However, several groups of bacteria have been known to be obligate degraders of hydrocarbons, namely, Alcanivorax, Cycloclasticus, Oleispira, Oleiphilus and Thalassolituus. Although other groups like Marinobacter and Pseudomonas have also shown versatile properties of degrading hydrocarbons (5, 6).

Species Isolated at Author
Halanaerobium, Sphingomonas, Afipia, Roseobacter and Pseudomonas Camargue (France) Bordenave et. al (2007) (7)
Pseudomonas, Shewanella, Vibrio, Alcanivorax, Marinobacter, Acinetobacter, Bacillus, Halomonas, Microbulbifer, etc. Gulf of Mexico (USA) Kostka et. al (2011) (8)
Methylophaga, Marinobacter, Martelella, Stappia, Paracoccus, Alkanivorax, Roseovarius, etc. A Coruña (Spain) Vila et. al (2010) (9)
Marinobacter, Shewanella, Pseudomonas Arctic Sea Gerdes et. al (2005) (10)

Oil-degrading bacterial community composition of few studies

With respect to oil hydrocarbons, the wide spectrum of over 17,000 compounds can be divided into four classes, Resins (quinolones, sulfoxides, amides and pyridines), Asphaltenes (Ketones, fatty acids, esters and phenols), Saturates and Aromatics (11). During hydrocarbon degradation processes, the alkanes are degraded fast. On the other hand polycyclic aromatic hydrocarbons (PAHs) are degraded least efficiently owing to their hydrophobicity and high molecular weights (12).

Microbial process of oil hydrocarbon degradation

Overall, the microbial process of oil hydrocarbon degradation has been divided into two main groups of processes, aerobic and anaerobic. Using a wide range of electron source, where aerobic processes are rapid and lead to complete metabolism of the substrates.

Various types of enzymes which led to the microbial degradation of oil in case of oil spills

Different classes of enzymes involved in microbial degradation of oil hydrocarbons (Source: Das and Chandra (2011))

Microbial aerobic oxidation of oil hydrocarbons utilizes oxygen for oxidation of hydrocarbon and terminal electron acceptor of respirator electron flow. It also requires the action of enzymes and bio-surfactants (6,13). Das and Chandra (2011) identified several groups of enzymes that are present in different oil-degrading species and help in metabolism of different compounds. The main process of enzymatic degradation of oil hydrocarbons involves two steps:

  1. Initial attack by membrane-bound or intracellular oxygenases and peroxidases where the hydrocarbon is activated and oxygen is incorporated.
  2. Peripheral degradation pathways, where the hydrocarbons are degraded in multiple steps to substrates of important central intermediary metabolism pathways like the TCA cycle (6,14). Consequently, the hydrocarbons are utilized by the microbes for respiration as well as for biosynthesis.
Groups of Biosurfactants produced by oil-degrading microbes after oil spills

Major groups of Biosurfactants produced by oil-degrading microbes (Source: Das and Chandra (2011))

Importance of biosurfactants as oil spill bioremediation

Furthermore, biosurfactants synthesized by microbes play a monumental role in the degradation of oil spill in the natural environment. Therefore it has been a subject of oil spill bioremediation agents’ research. These chemicals are a group of surface active compounds (as shown in the above figure). They are capable of reducing surface and interfacial tensions. These also assist microbes in increasing the stability and bioavailability of hydrophobic hydrocarbon substrates by emulsifying them (15). Microbial biosurfactants help in bioremediation of hydrophobic compounds by two main mechanisms. The first one is increasing the surface area through emulsification. Secondly, increasing the bioavailability (by micelle formation or decreasing interfacial tension and increasing solubility) of hydrophobic water insoluble substrates (14).

To initiate degradation, bacteria is required to come in close contact with the oil substrate. This can be either by emulsification of hydrophobic hydrocarbons or by growing high molecular weight polymers that help bind to the surface. Thus it ensures cell membrane-bound oxygenases access to the substrate (14). As a result, hydrophobic oil substrates that were initially limiting biodegradation processes due to low bioavailability, can now be metabolized by the microorganisms. However, oil spill bioremediation also suffers from another limiting factor, in the form of complex chemical nature of the oil, which results in varying susceptibility to microbial attack. This is due to the fact that oil typically consists of different quantities of saturates, aromatics, asphaltenes and resins. Microbes show varying activity against each of these types of hydrocarbon compounds, such that some are easily degradable (alkanes), while others like Polycyclic Aromatic Compounds (PAHs) are very hard to degrade (6). Such recalcitrant compounds, not capable of degradation, may continue to exist in the environment, without any signs of removal.

The next article in this series focuses on another important hydrocarbon pollutant, plastics. Plastics, due to their inherent properties, are highly stable and are resistant to chemical and physical degradation. Moreover, the mounting presence of plastic wastes in marine environments have increased pressure on scientists and policymakers to mitigate this pollution.

References

  1. Wang Z, Stout S. Oil Spill Environmental Forensics: Fingerprinting and Source Identification. San Diego: Academic Press; 2010. 620 p.
  2. ITOPF. Oil Tanker Spill Statistics 2015 [Internet]. 2016. Available from: http://www.itopf.com/fileadmin/data/Documents/Company_Lit/Oil_Spill_Stats_2016.pdf
  3. Moss L. The 13 largest oil spills in history [Internet]. Mother Nature Network. 2010. Available from: http://www.mnn.com/earth-matters/wilderness-resources/stories/the-13-largest-oil-spills-in-history
  4. Bordenave S, Goñi-Urriza MS, Caumette P, Duran R. Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Appl Environ Microbiol [Internet]. American Society for Microbiology; 2007 Oct [cited 2016 Nov 30];73(19):6089–97. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17704271
  5. Brooijmans RJW, Pastink MI, Siezen RJ. Hydrocarbon-degrading bacteria: the oil-spill clean-up crew. Microb Biotechnol [Internet]. Blackwell Publishing Ltd; 2009 Nov [cited 2016 Dec 1];2(6):587–94. Available from: http://doi.wiley.com/10.1111/j.1751-7915.2009.00151.x
  6. Das N, Chandran P. Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int. 2011;2011:1–13.
  7. Bordenave S, Goñi-Urriza MS, Caumette P, Duran R. Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Appl Environ Microbiol [Internet]. American Society for Microbiology; 2007 Oct [cited 2016 Nov 30];73(19):6089–97. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17704271
  8. Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A, et al. Hydrocarbon-degrading bacteria and the bacterial community response in gulf of Mexico beach sands impacted by the deepwater horizon oil spill. Appl Environ Microbiol [Internet]. American Society for Microbiology; 2011 Nov [cited 2016 Nov 30];77(22):7962–74. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21948834
  9. Vila J, Nieto JM, Mertens J, Springael D, Grifoll M. Microbial community structure of a heavy fuel oil-degrading marine consortium: linking microbial dynamics with polycyclic aromatic hydrocarbon utilization. FEMS Microbiol Ecol [Internet]. Blackwell Publishing Ltd; 2010 May 7 [cited 2016 Nov 30];73(2):no – no. Available from: http://femsec.oxfordjournals.org/cgi/doi/10.1111/j.1574-6941.2010.00902.x
  10. Gerdes B, Brinkmeyer R, Dieckmann G, Helmke E. Influence of crude oil on changes of bacterial communities in Arctic sea-ice. FEMS Microbiol Ecol [Internet]. Blackwell Publishing Ltd; 2005 Jun [cited 2016 Nov 30];53(1):129–39. Available from: http://femsec.oxfordjournals.org/cgi/doi/10.1016/j.femsec.2004.11.010
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  12. Atlas R, Bragg J. Bioremediation of marine oil spills: when and when not – the Exxon Valdez experience. Microb Biotechnol [Internet]. Blackwell Publishing Ltd; 2009 Mar [cited 2016 Dec 1];2(2):213–21. Available from: http://doi.wiley.com/10.1111/j.1751-7915.2008.00079.x
  13. Prince R, Garrett R, Bare R, Grossman M. The roles of photooxidation and biodegradation in long-term weathering of crude and heavy fuel oils. Spill Sci Technol Bull [Internet]. 2003 [cited 2016 Dec 1];8(2):145–56. Available from: http://www.sciencedirect.com/science/article/pii/S1353256103000173
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  15. Mukherjee S, Das P, Sen R. Towards commercial production of microbial surfactants. Trends Biotechnol. 2006;24(11):509–515
Chandrika Kapagunta

Chandrika Kapagunta

Research Analyst at Project Guru
Chandrika is a nature enthusiast with special love for the marine world. Her Master’s degree in Marine Biotechnology and Scuba Diving experience has made her a strong advocate of environment and marine conservation, especially through bioremediation. She believes in finding solutions of everyday human problems in nature, be it medicines, technology or philosophy. Having worked as a volunteer at The Bombay Natural History Society and as a Senior Research Fellow at Central Institute of Fisheries Education, she has had exposure to the current state of the academic research, specifically in the field of environmental biotechnology.
Chandrika Kapagunta

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