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  • Review Article
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Marine microorganisms make a meal of oil

Nature Reviews Microbiology volume 4, pages 173–182 (2006)Cite this article

Key Points

  • Hydrocarbons enter the environment from many sources, including marine algae and natural hydrocarbon seeps, as well as anthropogenic sources that are associated with the production, transport and use of crude oil. It is therefore unsurprising that there are numerous microorganisms that can use hydrocarbons as a source of carbon and energy.

  • Crude oil is perhaps the most complex mixture of organic chemicals that is found on Earth. Some components are readily biodegraded (for example, many saturated hydrocarbons), whereas others are more persistent and toxic (for example, high-molecular-weight polycyclic aromatic hydrocarbons and polar components of crude oil such as benzofurans, benzocarbazoles and benzothiophenes). The most important by mass are the relatively readily degradable saturated hydrocarbons.

  • Considerable knowledge of the detailed biochemistry and molecular basis for the biodegradation of aliphatic and simple aromatic hydrocarbons has been accrued. However, the importance in natural environments of the degradative organisms that have been studied in the laboratory is less clear. Only recently have we begun to learn which bacteria are of particular importance in hydrocarbon degradation, especially in marine environments.

  • Several specialist hydrocarbon-degrading bacteria have now been isolated and shown to be numerically important during the biodegradation of crude oil in marine environments. The identity of these bacteria and their distribution and dynamics in the environment are discussed in this article.

  • The degradation of hydrocarbons in the environment relies on much more than the hydrocarbon-degrading bacteria themselves. The effects of environmental conditions and interactions with other organisms — both positive and negative — are explored.

  • The potential for ecological theory to explain the patterns and dynamics seen in microbial communities that are associated with hydrocarbon degradation is discussed in relation to resource partitioning between community members, mutualistic interactions between hydrocarbon degraders and non-degraders, and predation.

  • A future perspective is presented that relates our vast body of knowledge gained from traditional biochemistry and molecular biology to the opportunities presented by the advent of genomic and post-genomic technologies. Suggestions are made about how the characteristics of hydrocarbon-degrading communities make them well-suited to hypothesis-led metagenomic studies to increase our understanding of how different components of a microbial community that is associated with hydrocarbon degradation interact to achieve effective exploitation of hydrocarbons.

Abstract

Hundreds of millions of litres of petroleum enter the environment from both natural and anthropogenic sources every year. The input from natural marine oil seeps alone would be enough to cover all of the world's oceans in a layer of oil 20 molecules thick. That the globe is not swamped with oil is testament to the efficiency and versatility of the networks of microorganisms that degrade hydrocarbons, some of which have recently begun to reveal the secrets of when and how they exploit hydrocarbons as a source of carbon and energy.

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Figure 1: The effects of biodegradation on oil composition.
Figure 2: A phylogenetic tree illustrating the diversity of aerobic hydrocarbon-degrading bacteria.
Figure 3: Changes in the composition of spilled oil and corresponding changes in the abundance of key organisms.
Figure 4: A microbial degradation network.
Figure 5: The effect of nutrients on Alcanivorax spp.

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Acknowledgements

We are grateful to the Biotechnology and Biological Sciences Research Council (United Kingdom) and to our colleagues at AEA Technology plc (Didcot, Oxfordshire, United Kingdom), who have supported our work on hydrocarbon-degrading microbial communities. W.F.M.R. is supported by The Netherlands BSIK (Besluit Subsidies Investeringen Kennisinfrastructuur) Ecogenomics Research Programme. Information on the thickness of the oil layer that could form on the oceans from oil released from natural seeps (see Abstract) comes from Ref. 2.

Author information

Authors and Affiliations

  1. School of Civil Engineering and Geosciences, University of Newcastle upon Tyne, Newcastle upon Tyne, NE1 7RU, UK

    Ian M. Head & D. Martin Jones

  2. Department of Molecular Cell Physiology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, De Boelelaan 1085, Amsterdam, 1081 HV, The Netherlands

    Wilfred F. M. Röling

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  1. Ian M. Head
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DATABASES

Entrez Genome Project

Alcanivorax borkumensis

Burkholderia fungorum

Burkholderia mallei

Burkholderia pseudomallei

Geobacter metallireducens

Legionella pneumophila

M. avium subsp. paratuberculosis

Mycobacterium avium

Mycobacterium bovis

Mycobacterium smegmatis

Mycobacterium tuberculosis

Pseudomonas aeruginosa

Pseudomonas putida

Silicibacter pomeroyi

Wolinella succinogenes

Entrez Nucleotide

AB166953

AF062642

FURTHER INFORMATION

Microbial ecology, at the University of Newcastle upon Tyne

The Netherlands BSIK Ecogenomics Research Programme

Glossary

Hydrocarbons

Organic compounds that contain only carbon and hydrogen.

Bioremediation

The use of biological organisms such as plants or microorganisms to aid in the removal of hazardous substances from a polluted area.

Laboratory microcosm

A laboratory incubation system that is designed to simulate environmental conditions. This can be as simple as a flask or serum bottle, or it can be more complex (for example, a system that incorporates diurnal and tidal cycles).

Community dynamics

Changes in community size and composition that result from various forces (such as climate changes, nutrient concentrations, habitat destruction, predation and so on) that control and regulate communities over time.

Chao1

A non-parametric statistic that allows the species richness of an environment to be estimated by analysis of data from a small sample.

Interstitial waters

The water that surrounds sediment particles in aquatic environments. The composition of interstitial waters is controlled by the physical, chemical and biological activity of the sediment.

Phenanthrenes

Readily biodegradable, relatively water-soluble polycyclic aromatic compounds that are found in crude oil. Phenanthrene, the parent molecule, is a tri-aromatic hydrocarbon, and substituted phenanthrenes have alkyl substitutions of varying number and position on the aromatic rings.

Dibenzothiophenes

Sulphur-containing, non-hydrocarbon compounds that are found in crude oils. Dibenzothiophene, the parent molecule, comprises two benzene rings linked by a carbon–carbon bond and has a sulphur bridge between adjacent carbon atoms on the benzene ring. Crude oil contains a diverse mixture of such compounds with a variety of substitutions on the benzene rings.

Phylogenetic microarray

A microarray 'printed' with a range of marker genes or oligonucleotides (often including ribosomal-RNA-gene sequences) that is diagnostic for specific microbial taxa. Such arrays can be used to track the simultaneous presence of many microbial taxa.

Eutrophication

Enrichment of an environment with nutrients such that algal blooms and other negative environmental effects occur.

Syntrophy

A close metabolic interaction between different groups of organisms. The term is usually used with respect to interspecies hydrogen transfer in anaerobic systems.

Surfactant

A surface-active agent that reduces the surface tension of two liquids: for example, an agent that functions as a dispersant or emulsifier of oil and water.

Bioaugmentation

The addition of non-native microorganisms to polluted sites to clean up toxic wastes.

Metagenomics

The study of microbial genome fragments that are recovered from environmental samples, in contrast to genomes that are isolated from clonal cultures.

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Head, I., Jones, D. & Röling, W. Marine microorganisms make a meal of oil. Nat Rev Microbiol 4, 173–182 (2006). https://doi.org/10.1038/nrmicro1348

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